1. bookVolume 58 (2019): Issue 4 (January 2019)
Journal Details
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Journal
eISSN
2545-3149
First Published
01 Mar 1961
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English, Polish
access type Open Access

Edaphic Factors And Their Influence On The Microbiological Biodiversity Of The Soil Environment

Published Online: 31 Dec 2019
Volume & Issue: Volume 58 (2019) - Issue 4 (January 2019)
Page range: 375 - 384
Received: 01 Sep 2019
Accepted: 01 Oct 2019
Journal Details
License
Format
Journal
eISSN
2545-3149
First Published
01 Mar 1961
Publication timeframe
4 times per year
Languages
English, Polish
Abstract

The edaphic factors are the soil properties that affect the diversity of organisms living in the soil environment. These include soil structure, temperature, pH, and salinity. Some of them are influenced by man, but most are independent of human activity. These factors influence the species composition of soil microbial communities, but also their activity and functionality. The correlations between different abiotic factors and microbial groups described in this manuscript indicate both the complexity of the soil environment and its sensitivity to various stimuli.

1. Introduction. 2. Soil type and structure. 3. Soil pH and salinity. 4. Soil temperature. 5. Soil moisture. 6. Organic carbon and nitrogen content. 7. Heavy metals content. 8. Conclusions

Key words

Słowa kluczowe

Introduction

Soil microbiome includes all saprophytic microorganisms, commensals and parasites that inhabit the soil. It is estimated that one gram of fresh fertile soil matter can contain up to billions of bacteria [53]. The taxonomic and functional diversity of microorganisms and their interactions affect the functioning of the whole soil ecosystem. Many species complement each other and form a system responsible for soil processes. The functional diversity of soil microbiomes is related to the proper functioning of terrestrial ecosystems. The diversity of microorganisms in the soil environment depends on the physical and chemical properties of the soil and, indirectly, on the anthropogenic factors that influence them.

Ecological (environmental) factors are divided into abiotic and biotic. This study is concerned with abiotic factors, i.e. inanimate elements of the environment, which affect the functioning of living organisms directly or indirectly. They are chemical and physical parts of the environment. The whole range of soil conditions affecting the life of soil organisms is called edaphic factors. They are distinguished as a separate group of abiotic factors according to the importance of soil in terrestrial ecosystems. They are prerequisites for the existence of specific habitat conditions and, as a result of the specific composition of the community of the organisms that inhabit them [35].

Among the edaphic factors related to the soil we can distinguish (Fig. 1.):

soil structure and type,

soil temperature,

soil moisture,

soil pH and acidity,

mineral salt content (salinity).

Fig. 1.

Types of ecological factors.

Shelford’s universal ecological law says that the optimal development of any organism depends on the balance of a complex of environmental factors [36]. The ecological tolerance is a range of any factor (abiotic or biotic) in which the organism can exist, i.e. perform physiological processes. However, the maximum growth, activity and reproduction of each organism take place within the limits of the optimum occurrence of a given environmental factor (Fig. 2). This also applies to soil microorganisms.

Fig. 2.

General ecological tolerance curve of the species. Based on Lynch and Gabriel [45].

The availability of water, temperature and salinity vary the types of soil microorganisms and create frontiers, in which the microorganism can survive and affect competition between species. Edaphic properties are the basic ecological filter affecting the structure of soil microbiomes [9].

Many previous studies of microorganisms based on microbiological cultures on a specific medium, which eliminated a large part of microorganisms that are defined as an uncultured [51]. However, it is now known that only 1% of soil microorganisms can be isolated using traditional methods [15]. For this reason, modern techniques, including molecular biology, are increasingly present in soil microbiology research. In recent years metagenomics has developed. It is a method of genome analysis consisting of all microorganisms inhabiting the environment [76]. Modern research methods allow us to explore the influence of various environmental factors on soil microorganisms [18]. Researchers use them to analyze the impact of the environment on the diversity of soil microorganisms. Some research concerning the influence of edaphic factors on soil microbiome is presented in this review.

The aim of this review is to determine the existing knowledge on the most important abiotic factors influencing soil microorganisms and to highlight the importance of modern research methods in the identification of soil microbiological biodiversity.

Soil type and structure

Soil structure includes the size, shape, and arrangement of particles such as sand, silt, and clay [39]. It was shown that micro-grained soils usually contain higher amounts of microbial biomass than coarse-grained soils. It was found that the lighter soil structure favoured the development of bacteria [4]. Researchers indicate that clay molecules and a higher number of micropores in fine-grained soil limit the development of mesofauna, which protects microorganisms from predation [50]. Meliani et al. [50] showed that bacterial abundance was correlated with soil fractions, while no correlation between fungal abundance and fractions was observed. Using Terminal-Restriction Fragment Length Polymorphism (T-RFLP) analysis researches found dominant associations of Alphaproteobacteria to large soil particles (i.e. sand) and Halophaga and Acidobacterium associations with smaller soil’s particles (i.e. clay) [66].

With the use of classical microbiological methods, i.e. culture on media, the research on 18 soil types in Georgia showed that soils differ in their total bacterial abundance and in the prevalence of some types of bacteria such as Bacillus, Pseudomonas and Rhodocococcus [17]. It was found that brown, chernozem and marshy soils are the richest in terms of bacterial abundance. Bacillus bacteria dominate in the majority of soils studied by researchers, Pseudomonas bacteria were the most abundant in alluvial and brown forest soils, while Rhodocococcus sp. is common in yellow-brown and red forest soils. In the course of research conducted on eight types of Polish soils by Grządziel and Gałązka [26] using the next generation sequencing (NGS; MiSeq, Illumina), a ten types of bacteria common to all eight soils were selected: Conexibacter, Bacillus, Saccharopolyspora, Rhodoplanes, Azospirillum, Paenibacillus, Streptomyces, Gemmatimonas and Mycobacterium. The analysis of the microbiome of the chickpeas rhizosphere growing on different soil types in the same climate also showed that microbiomes differ from soil to soil [47]. This eubacterial community structure was examined by denaturing gradient gel electrophoresis (DGGE), and the authors have concluded that the bacterial community structure in the rhizosphere as affected by a complex interaction between soil type and plant species. In different soil types under lettuce cultivation subjected to the same agrotechnical treatments and identical climatic conditions, bacterial differentiation depending on the soil type was found [65]. Kuramae et al. [38] using the PhyloChip analysis, which is the high-density DNA microarray, also indicate that some bacterial taxa are strongly correlated with the physicochemical properties of the soil.

The determination of an unequivocal influence of soil type and type on the structure of microbial communities is a difficult issue because of the complexity of taking into account many variables (minerals, texture, pH, physical structure, etc.) when comparing different soils.

Soil pH and salinity

The soil pH depends on the type of rock from which the soil was formed. Acid soils are formed from igneous rocks and sands. Alkaline soils are formed from carbonate rocks (e.g. limestone). In addition, the pH of the soil is influenced by climate, rock weathering, organic matter and human activity [21]. The soils are strongly acidic (pHKCL < 4.5), acidic (pHKCL 4.5 – 5.5), slightly acidic (pHKCL 5.6 – 6.5), neutral (pHKCL 6.6 – 7.2) and alkaline (pHKCL > 7.2) [23]. In Poland, the soil pH ranges from 3.0 to 8.5. The lowest pH is found in non-carbonate forest soils and the highest in carbonate soils [23].

The impact of various factors on the composition of soil microorganisms was investigated using 16S V4–5 region sequencing (HiSeq, Illumina) and it was shown that soil pH has a significant influence on the development of specific bacteria [57]. Researchers showed, that soil pH significantly correlated with such bacteria phyla as Acidobacteria, Beta-Proteobacteria and Bacteroidetes. In another study, using NGS, it was also shown that the pH is often identified as the main factor affecting, in particular, the bacterial communities and archaea [9]. Different groups of microorganisms have distinct limits for optimal pH, so that acidic, neutral and alkaline soils have a different microbial structure, both in terms of quantity and diversity of the population. The pH value indirectly affects the structure of microbial communities, also by influencing the availability of nutrients in the soil [57]. Most soil microorganisms prefer a pH close to neutral (6–7). However, there are also those adapted to extreme pH values, i.e. acidophiles and alkalophiles. Acidophilic microorganisms develop in very acidic environments at pH 3.0 or lower. These are, among others, bacteria from genera: Acidithiobacillus, Thiobacillus, Acetobacter, Alicyclobacillus and some species from the Acidobacteria. Archaea representatives were isolated from dry soil (Japan) with extremely low pH: Picrophilus torridus and P. oshimae, which develop at pH 0.7 [59]. Alkalophiles grow optimally at pH above 9.0, which is found in desert sodium soils (e.g. in the west of the United States). Among the alkalophilic microorganisms present in the soil one can distinguish the representatives of the genera Bacillus, Flavobacterium, Methanobacterium, and Corynebacterium. Extreme alkalophilic actinomycete strain isolated from desert soil in Egypt consistently to the genus Nocardiopsis, which was confirmed by 16S rDNA analysis and researchers proposed name N. alkaliphila. This bacterium grows at pH between 7.0 and 12.0 [30].

Analysis of soil Phospholipid Fatty Acid (PLFA) showed that low pH can increase the total abundance of fungi in the soil fivefold, with a simultaneous decrease in the number of bacteria [62]. They are preferable to pH between 4 and 6, and some of them, such as Saccharomyces, Aspergillus, Penicillium or Trichosporon, are even acidophilic [34]. Grządziel and Gałązka [26] showed that the soil with the lowest pH analyzed (4.0; Brunic Arenosol I) was characterized by a different microbiome than the other seven soil types. In the Dutch soils, a strong correlation was found between the number of Bacilli and Clostridium groups with soil pH and phosphorus content [38]. The metagenomic DNAs from soil bacteria analysed by pyrosequenced revealed that in acidic soils (≤6.5) a higher diversity and the total number of bacteria was observed in comparison with soils with neutral pH (7.7) [6]. The T-RFLP analyses of soil samples from North and South America also showed that pH is a very important factor influencing the diversity and abundance of soil microorganisms. However, the researchers noted a lower bacterial diversity in acidic soils compared to neutral soils [14]. The effect of pH on the microbial community is already noticeable at broad levels of taxonomic resolution. Zhang et al. [81] using high-throughput sequencing observed that the abundance of actinobacteria, Bacteroidetes, Fibrobacteres and Firmicutes was higher at close to neutral pH and much lower at acidic and alkaline pH. Acidobacteria, Chloroflexi and Planctomycetes bacteria were abundant in acidic pH soil, then in neutral pH their number decreased and in alkaline pH slightly increased. The number of bacteria from the genera Gemmatimonadetes, and Nitrospirae [81] increased linearly with the increase in pH of the soil. One of the most pH-sensitive processes in the soil is nitrification. The conversion of ammonium ions (NH4+) to nitrates (NO3) is dependent on the alkalophilic bacteria Nitrobacter and Nitrosomonas, which optimally increase at pH 7.6–8.8 and are very sensitive to changes in pH [34]. At the same time, the nitrification process affects the pH of the soil, as, during the uptake of NH4+ ions by microorganisms, the environment becomes acidified, and during the uptake of NO3 ions by bacteria, the soil becomes alkaline [34]. The balance between the two stages of the nitrification reaction allows a constant pH of the soil to be maintained.

In addition to the soil reaction, the salinity level is very important for soil microorganisms. The main soil-soluble salts are sodium, calcium, magnesium and potassium cations and chlorine anions. The salinity of the soil solution affects the osmotic potential and the structural stability of the soil [78]. Depending on electrical conductivity (EC), sodium adsorption ratio (SAR) and pH, the soil is divided into three groups according to USDA (United States Department of Agriculture) classification:

saline soils – EC > 4,0 dS m–1, pH < 8,5, SAR < 13;

sodium soils – EC > 4,0 dS m–1, pH < 8,5, SAR > 13;

saline-sodium soils – EC < 4,0 dS m–1, pH > 8,5, SAR > 13.

The soil may be salted naturally and anthropologically. This applies to soils where the parent material is rich in soluble salts. Secondary salinity is the result of human activity. It is associated with poor irrigation and drainage of the soil, chemical contamination and incorrect fertilization [78]. High concentrations of salt ions (e.g. Na+, Cl) are harmful to plants, and salinity itself reduces the activity of microorganisms and changes their activity [2]. Osmotic stress caused by salinity causes cells to be dried out and lysed. Thus, the content of microbial biomass in the soil is also reduced [60]. Fungi are more susceptible to salt stress than bacteria, and therefore a higher bacterial-to-fungi ratio is observed in saline soils [74]. Some microorganisms have the ability to adapt or tolerate salinity in soil by synthesis and accumulation of osmolytes (e.g. proline, betaine, ectoine). Microorganisms called halophytes are particularly suited to high salt concentrations in the soil and produce enzymes resistant to salt and accumulate salt in their cells in quantities corresponding approximately to extracellular concentrations. Such microorganisms include Halobacteriaceae (archaea) and Salinibacter ruber (bacterium) [69]. Moreover, salinity was identified as the major factor of microbial community composition. Lozupone and Knight [44] research were based on an analysis of 21,752 RNA sequences isolated from 111 environmental samples from soils, sediments and water. Comparing the composition of the bacterial community in the analyzed samples, the researchers determined that salinity is the main determinant of microbiome composition and not the extremes of temperature and pH or other physical and chemical factors. Additionally, it was found that sediments are more phylogenetically differentiated than soil, which has high species-level diversity. Among the sequences obtained, many of them belonged to unnatural bacteria, and more than half of them were not related to literature reports. This indicates the importance of metagenomic studies in the context of environmental microbiology [44].

Soil temperature

Temperature is one of the most important edaphic factors determining the limits of microbial development because groups of microorganisms grow at the optimal temperature, and after exceeding this limit their growth is terminated [48]. Soil temperature affects not only the activity of microorganisms but also seed sprouting, root growth and availability of nutrients. Soil temperature depends on the sunlight reaching the ground surface, water content, terrain topography, air temperature, soil properties and the vegetation [61]. Dry soils quickly warm-up, but also lose heat quickly. Moisture soils maintain their temperature longer, and heat is quickly transferred to the deeper layers. In the summer months, the deeper layers of soil are heated and cooled in the winter months. In 1961–1975, the average annual soil temperature in Poland was 8.9°C, at a depth of 5 cm and in the growing season 14.7°C [61]. As a result of the Ciaranek [7] research, it was found that in the years 2007–2009 in Krakow (Poland) the annual average soil temperature at the same depth was 11.7°C; to the depth of 20 cm it fell (to 11.1°C), and to the depth of 50 cm it again amounted to 11.7°C.

The microorganisms are divided into different groups depending on the temperature optimum: (1) psychrophiles which grow best in an environment below 10°C; (2) mesophiles which are the majority of soil bacteria and have the highest growth rate in the 20–45°C range; (3) thermophiles which grow at 50–65°C [52]. Psychrophilic soil microorganisms occur in the soils of eternal permafrost [77]. These include bacteria (e.g. Halobacterium lacusprofundi, Sphingobacterium antarcticus), fungi (e.g. Penicillium jamesonlandense) and archaeons (e.g. Methanosarcina sp.). Based on psychrotrophs, a microbiological consortium was developed: Eupenicillium crustaceum, Paecilomyces sp., Bacillus sp. and B. atrophaeus potentially used in agriculture to increase soil fertility [68]. In geothermally heated regions, e.g. volcanic soils, there are microorganisms called hyperthermophiles with an optimum growth rate of 80–113°C [31]. They belong to bacteria and archaea, the vast majority of which are archaea. Two species of Picrophilus bacteria have been isolated from dry, volcanic soils in Japan, which grow at 60°C while tolerating pH 0.7 [59].

Changes in soil temperature affect the diversity of the microbiome. The use of next generation sequencing (HiSeq, Illumina), has shown that an increase in soil temperature (up to 58°C) as a result of a continuous underground fire of coal mines located under the surface of the city Centralia (Pennsylvania, United States) caused a reduction in the diversity and number of microorganisms and a decrease in the number of antibiotic resistance genes in soil [11]. Researchers, also using 16S rRNA gene sequencing, found that the soils affected by the fire are highly dominated by a small number of taxonomic microbial units [40]. Temperature also influences the activity of enzymes secreted by microorganisms into the soil environment. It was shown that an increase in temperature stimulates the activity of nitrogenase, an enzyme produced by diazotrophs bacteria that participates in the atmospheric nitrogen fixation [8]. Climate change, including an increase in temperature, also affects the structure and functioning of soil microorganisms [41]. Both, NGS (MiSeq, Illumina) and EcoPlate™ (Biolog Inc., Hayward, USA) methods were used in the research. Studies based on soil heating (mean soil temperature increase of 2.3°C) have shown that environmental warming has a significant impact on the metabolic potential of microorganisms. In heated soils, amines and carboxylic acids were rapidly decomposed [41]. In addition, it was demonstrated that soil heating has a significant effect on the soil fungal community and results in a decrease in the number of soil fungi to a greater extent than in the case of bacterial communities. Also with the use of classical analytical methods (soil respiration, soil biomass), it was shown that warming lasting longer than 3 years significantly affects the biomass of soil microorganisms [16]. Research using a combination of different research methods – both older and more recent (EcoPlate™, soil microbial biomass, PLFA) – has shown that microorganisms are able to adapt to a soil temperature increase of 1 to 2°C without disturbing the microbial structure [80].

An increase in temperature can also have the effect of dehumidifying the soil and reducing soil moisture, which is also an important edaphic factor affecting soil microorganisms.

Soil moisture

Soil moisture is defined as the water content of the soil. It is one of the most important physical parameters in agriculture, as it directly influences the growth of plants. A certain amount of water is stored in the soil. The water content of soil varies in time and space [78]. It depends on the soil properties, the type of vegetation, the intensity of evaporation (thus indirectly also on temperature), the amount and distribution of rainfall and irrigation in the case of arable land [54]. In Poland, precipitation is the primary source of water in soil [33].

Soil moisture affects the organisms living in the soil in many ways. Without the availability of water, microbial life is impossible. The water content of the soil affects the pH, the diffusion of solvents and gases and the availability of nutrients [75]. Water also enables the migration of microorganisms in the soil and the diffusion of compounds between the cells of organisms and the environment and is part of hydrolysis processes, and its content determines the rate of mineralization [34, 78].

Natural fluctuations in moisture associated with seasonal changes and precipitation are an important environmental factor in the metabolism of microorganisms. Recently, however, the frequency of floods and periodic flooding in Poland has been increasing and drought periods have been prolonged. Water stress caused by these phenomena affects soil microorganisms [79]. Some bacterial groups are very sensitive to alternating drainage and flooding conditions. These include, inter alia, autotrophic ammonia-oxidizing bacteria, which was confirmed by an analysis of 491bp segment of the amoA gene [19]. The researchers created the term water activity in the environment (aw), which determines the ratio of the partial pressure of soil solution to the partial pressure of clean water and can be used to determine the water demand of microorganisms [37]. It is assumed that chemically pure water has aw =1.

Bacteria and archaea usually require more water activity to grow than fungi. Most bacteria require to grow aw > 0.91, while most fungi and yeasts can grow at aw < 0.80 (Tab. I).

Minimum value of water activity in the environment for various microorganisms

Water acivity (aw)Microorganisms
1.00Caulobacter, Spirillum
0.98Pseudomonas, Clostridium
0.95Gram-negative bacteria
0.91Bacillus, Lactobacillus
0.88Saccharomyces, Candida
0.85Selected filamentous fungi (e.g. Penicillium)
0.80Part of the yeast
0.75Most of the filamentous fungi (e.g. Aspergillus, Monascus)
0.60Halophytes (e.g. Vibrio, Halomonas, Paracoccus)

Based on Libudzisz et al. [43] and Kunicki-Goldfinger [37].

The physical parameter – soil water potential (pF) [3] – is distinguished in the studies of the soil environment. The pF value of 0.00 corresponds to the full water capacity, which means that all soil pores are filled with water and pF = 4.2 is the point of permanent wilting of plants. In terms of soil water potential of soil microorganisms needed for development, microorganisms can be divided into three main groups:

Hygrophiles – developing at pF below 4.85 – bacteria, selected fungi;

Mesohygrophiles – developing at high pF but up to 5.48 – most fungi;

Xerophiles – capable of growth at a pF greater than 5.48 – some species from genera Aspergillus and Monascus.

The potential above which microbiological processes are no longer found is pF = 5.68 [3]. The highest values of microbiological activity in the soil are found at water potential of pF value between 2 and 4. The studies showed that the most optimal moisture content for organotrophic bacteria is 20% of maximum water capacity (MPW), for Azotobacter and Actinomycetes 40%, and for fungi 60% of MPW [5]. At 20% MPW the highest activity of enzymes such as dehydrogenases, catalase or acid and alkaline phosphatases was also observed.

Drought, i.e. a decrease in the water content of the soil, may result in an increase in the osmotic pressure of the soil and the formation of a hypertonic solution, which results in the drying out of microbial cells and reduces their activity and growth [56]. Lack of water also reduces the processes of carbon and nitrogen mineralization [78]. Drying the soil increases its oxygenation [34]. Some microorganisms are able to survive in such conditions in the state of anabiosis [43], i.e. in the state of extreme decrease in life activity. It is known that fungi are able to exist at lower aw values than bacteria (Tab. I), for which the optimal aw value is 0.98–0.99. The increase in bacteria was also observed at low water activity in the environment (aw =0.75), but it concerned halophilic bacteria of the genera Halomonas, Parococcus and Vibrio. Halophilic microorganisms and those tolerating low water content have the same defence mechanism – they produce and accumulate osmolytes [78]. As the soil dries, access to nutrients is reduced. Restoring moisture in dry soil is linked to an increase in the number of microorganisms as a result of increased susceptibility to organic matter decomposition [75]. Moisture fluctuations occur naturally in soils in semidry and Mediterranean ecosystems, where the soil is often quickly wetted after long periods of drought [13]. Studies show that after 24 hours after irrigation of such dry soil, the maximum microbiological activity in the soil is observed [12]. However, with the increase in the number of drying and irrigation cycles, biomass and microbial activity in the soil decrease, nitrification is inhibited and fungal abundance is reduced, while the number of Gram-positive bacteria increases [78].

Excessive humidity caused by floods, melt or heavy rainfall also causes changes in the structure and activity of the soil microbiome. Increased humidity is associated with reduced oxygen and nitrogen diffusion in the soil [5] and the development of predators that feed on bacteria [34]. Under anaerobic conditions in the soil, the availability of micro and macro-elements is two to four times lower than in a well-oxygenated environment. In the structure of soil microbiome and its activity there are changes caused by soil flooding with water and oxygen loss [20]. Microorganisms start to use oxygen bound to e.g. NO3 and MnO2, which leads to a reduction in these forms. Excessive irrigation and the associated lack of oxygen intensifies the development of anaerobic microorganisms, which in turn reduces the oxidative-reduction potential and intensifies the processes of reduction and fermentation [34]. Nitrate, manganese, sulphate and iron forms are reduced [46]. Research using PLFAs indicate that with the loss of oxygen, the number of Gram-negative bacteria decreases and the number of Gram-positive bacteria in the soil increases [73]. Gram-negative fungi and bacteria normally occur in well-aerated soil layers. As a result of oxygen depletion, their number decreases [72, 73]. Among the anaerobic soil microorganisms are, among others, purple bacteria carrying out anaerobic photosynthesis – Rhodospirillum sp.; sulphate-reducing bacteria – Desulfovibrio sp., Desulfotomaculum sp.; and nitrogen-fixing bacteria – Clostridium sp.; as well as the representatives of archaea, who produce methane – Methanobacterium sp. [43]. As a result of the floods, a decrease in soil microbial biomass was observed and sulphate and nitrate-reducing bacteria were identified [72]. It was also found that the occurrence of intensive precipitation in vineyards increased the development of epiphytic microorganisms, including pathogenic fungi, e.g. Botrytis cinerea [63].

Organic carbon and nitrogen content

Soil organic matter is a basic indicator of soil quality, which determines its physicochemical properties and biological processes. High humus content in soils is, a factor stabilizing their structure, reducing susceptibility to compaction and degradation [49].

Carbon content plays an important role in the regulation of the diversity and structure of soil microbiome [82]. A research of 29 soil samples from four geographically distinct locations using a small-subunit (SSU) rRNA-based cloning approach demonstrated that carbon-poor soils had microbial composition shifts associated with soil depth [82]. It was shown, that deeper soil communities were less diverse and had strongly dominant genera, whereas surface communities had more an operational taxonomic unit (OTU). It was demonstrated, based on quantitative PCR (qPCR) of genes encoding the key enzymes of ammonia oxidation (amoA), nitrate reduction (narG) and denitrification (nirK, nirS, nosZ), that the forms of soil carbon (i.e. inorganic, organic) affects the structure of denitrification communities, but does not regulate their numbers [29]. Among the microorganisms preferring carbonrich environments (e.g. rhizosphere) based on bacterial and archaeal 16S rRNA sequenced, one can distinguish Alphaproteobacteria [28].

Nitrogen in soil is a mobile component that undergoes a number of environmental changes: ammonification, nitrification, denitrification or sorption. Many of these processes involve bacteria, so it is understandable that the amount of nitrogen in the soil determines the number of bacterial communities in the soil [70]. The source of nitrogen in the soil is both mineral and organic fertilization, decomposition of plant residues, as well as free nitrogen binding by symbiotic bacteria Rhizobium or free-living assimilators – Azotobacter, Arthrobacter, Beijerinckia, and Clostridium.

The type of nitrogen fertilizer used (e.g. urea, sewage sludge, ammonium sulphate, calcium nitrate, manure) has a significant effect on soil pH [27]. Fertilization with e.g. ammonium nitrate causes pH decrease in soil by as much as 1.4 and consequently affects the communities of soil bacteria, which was confirmed by pyrosequenced analysis [58]. The use of organic fertilizers increases the number of endophytic nitrifies in soil [55].

Heavy metals content

Heavy metals are naturally present in each soil at a non-hazardous level. However, exceeding certain standards is very harmful. Excessive concentrations of heavy metals in the soil are due to human activity, including, but not limited to, crop errors. Among heavy metals, there are harmful elements such as cadmium, lead, mercury, nickel and arsenic, but also high concentrations of zinc and manganese [1].

Using pyrosequencing, it was shown that in Polish soils zinc decreased both bacterial diversity and species richness. In soils contaminated by zinc, lead and chromium it was possible to delineate the core microbiome, which comprised members of such taxa as Sphingomonas, Candidatus Solibacter and Flexibacter [22]. Using the high-throughput Illumina sequencing of 16S rRNA gene amplicons it was determined also, that bacteria have different reactions to heavy metals. The bacteria that positively correlated with Cd were, among others, Acidobacteria Gp and Proteobacteria. A negative correlation was found in e.g. Longilinea. Analysis the effects of heavy metals on a soil microbial community using DGGE showed that exposing soil to heavy metals changed the microbial community structure representing dominant but also minor populations [25]. Based on the number and type of OTU obtained, the researchers found that the soil bacteria community can adapt to long-term heavy metal contamination through the change in microbial community composition and structure, rather than the change in their species diversity and evenness [42]. The metal-resistant bacteria include the genus Thiobacillus, which showed a significant positive correlation with cadmium, zinc, arsenic, and lead indicating that the genus was tolerant to heavy metal [42]. The study conducted on the paddy soils along a nonferrous smelter in South Korea showed, that the phylum Proteobacteria was found to predominate in all samples, regardless of the heavy metal concentration. Used the 16S rRNA gene pyrosequencing authors found, that only in the case of the phylum Chlorobi, a strong negative impact of the soil cadmium concentration was revealed [71]. Researchers concluded that the diversity in the bacterial community structure at the phylum level was mostly related to the general soil properties, while at the finer taxonomic levels, the concentrations of arsenic and lead were the significant factors affecting the community structure [71]. Analyses the bacterial community response to arsenic and chromium contamination revealed by pyrosequencing researchers showed that in non-contaminated soils the dominant phylum was Actinobacteria, whereas in contaminated soils it was Proteobacteria. In addition, in contaminated soils a decrease in OTUs number of 14–38% was observed in comparison to control soils. The decrease in bacterial diversity within the contaminated soils was confirmed by species richness (Chao, ACE, Shannon) based on pyrosequencing data [67]. The qPCR and PCR-DGGE analysis on samples from agricultural soils near manufacturing district suggests that heavy metal pollution has significantly decreased abundance of bacteria and fungi and also changed their community structure [10]. Researchers analysed the contaminated landfill soils of Peninsular Malaysia showed, that P. mendocina has the highest resistance to metal exposure. When B. pumilus was absolutely resistant to the heavy metals used in the study, except nickel [32]. Examination of lead-contaminated soils by high throughput amplicon sequencing showed that Verrucomicrobia were less abundant at high contamination level whereas Chlamydiae and γ-Proteobacteria were more abundant [64].

Unlike bacteria, in the research provided by Li et al. [42] the members of the archaeal domain, i.e. phyla Crenarchaeota and Euryarchaeota, class Thermoprotei and order Thermoplasmatales showed an only positive correlation with Cd. The researchers stated that archaea were resistant to heavy metal contamination and can contribute to its adaptation to heavy metal. Also in other environment contaminated with heavy metals (anoxic freshwater lake sediments) was found that Crenarchaeota was associated with metal contamination [24].

The presented researches indicate that the heavy metal content affects the distribution of microbial population in the soil. Some types are resistant or even prefer environments with high metal content, but most data indicate a decrease in the number and variety of microorganisms, especially bacteria, in soil with increased contamination.

Conclusion

The most important abiotic factors influencing soil microorganisms are described in this review. Apart from the edaphic factors described above, the soil nutrient content in available forms, toxic compounds, light and oxygenation can be distinguished. There are complex relationships between these factors since salinity affects the pH of the environment, temperature affects the water content of the soil, and both the presence of salt and humidity depending on the type of structure of the soil. The different taxonomic units of microorganisms are characterized by different ecological optimum. This is important from the point of view of agriculture, because human intervention in the soil environment may cause changes which will have a negative or positive impact on microorganisms. Microorganisms are known for their many adaptation mechanisms, but they still have environmental tolerance limits, beyond which they lose their viability or die. Maintaining constant conditions optimal for a given soil environment provides for the development and activity of the microbial community.

The use of new research methods in environmental microbiology allows for a more detailed examination of soil microbial contamination, but the vastness of the links between the various components of the soil environment is so great that much remains unknown.

Fig. 1.

Types of ecological factors.
Types of ecological factors.

Fig. 2.

General ecological tolerance curve of the species. Based on Lynch and Gabriel [45].
General ecological tolerance curve of the species. Based on Lynch and Gabriel [45].

Minimum value of water activity in the environment for various microorganisms

Water acivity (aw)Microorganisms
1.00Caulobacter, Spirillum
0.98Pseudomonas, Clostridium
0.95Gram-negative bacteria
0.91Bacillus, Lactobacillus
0.88Saccharomyces, Candida
0.85Selected filamentous fungi (e.g. Penicillium)
0.80Part of the yeast
0.75Most of the filamentous fungi (e.g. Aspergillus, Monascus)
0.60Halophytes (e.g. Vibrio, Halomonas, Paracoccus)

Alloway B.: Heavy Metals in Soils. Vol. 22, Springer, Dordrecht, 2013AllowayB.Heavy Metals in SoilsVol.22SpringerDordrecht201310.1007/978-94-007-4470-7Search in Google Scholar

Andronov E.E., Petrova S.N., Pinaev A.G., Pershina E.V., Rakhgimgalieva S.Zh., Akhmedenov K.M., Gorobets A.V., Sergaliev N.Kh.: Analysis of the structure of the microbial community in soils with different degrees of salinization using T-RFLP and real-time PCR techniques. Euras. Soil Sci. 45, 147–156 (2012)AndronovE.E.PetrovaS.N.PinaevA.G.PershinaE.V.RakhgimgalievaS.Zh.AkhmedenovK.M.GorobetsA.V.SergalievN.Kh.Analysis of the structure of the microbial community in soils with different degrees of salinization using T-RFLP and real-time PCR techniquesEuras. Soil Sci.45147156201210.1134/S1064229312020044Search in Google Scholar

Bednarek R., Dziadowiec H., Pokojska U., Prusinkiewicz Z.: Badania ekologiczno-gleboznawcze. Wydawnictwo Naukowe PWN, Warszawa, 2005BednarekR.DziadowiecH.PokojskaU.PrusinkiewiczZ.Badania ekologiczno-gleboznawczeWydawnictwo Naukowe PWNWarszawa2005Search in Google Scholar

Bonneau M., Souchier B.: Pedology: Constituents and soil properties. Masson Publisher, Paris, 1994BonneauM.SouchierB.Pedology: Constituents and soil propertiesMasson PublisherParis1994Search in Google Scholar

Borowik A., Wyszkowska J.: Impact of temperature on the biological properties of soil. Int. Agrophys. 30, 1–8 (2016)BorowikA.WyszkowskaJ.Impact of temperature on the biological properties of soilInt. Agrophys.3018201610.1515/intag-2015-0070Search in Google Scholar

Cho S.J., Kim M.H., Lee Y.O.: Effect of pH on soil bacterial diversity. J. Ecol. Environ. 40, 10 (2016)ChoS.J.KimM.H.LeeY.O.Effect of pH on soil bacterial diversityJ. Ecol. Environ.4010201610.1186/s41610-016-0004-1Search in Google Scholar

Ciaranek D.: Influence of weather conditions on the variation of soil temperature in the Botanical Garden of Jagiellonian University in Kraków. Prace Geograficzne, 133, 77–99 (2013)CiaranekD.Influence of weather conditions on the variation of soil temperature in the Botanical Garden of Jagiellonian University in KrakówPrace Geograficzne13377992013Search in Google Scholar

Das S., Bhattacharyya P., Adhya T.K.: Impact of elevated CO2, flooding, and temperature interaction on heterotrophic nitrogen fixation in tropical rice soils. Biol. Fert. Soils, 47, 25–30 (2011)DasS.BhattacharyyaP.AdhyaT.K.Impact of elevated CO2, flooding, and temperature interaction on heterotrophic nitrogen fixation in tropical rice soilsBiol. Fert. Soils472530201110.1007/s00374-010-0496-2Search in Google Scholar

de Gannes V., Eudoxie G., Bekele I., Hickey W.J.: Relations of microbiome characteristics to edaphic properties of tropical soils from Trinidad. Front. Microbiol. 6, 1045 (2015)de GannesV.EudoxieG.BekeleI.HickeyW.J.Relations of microbiome characteristics to edaphic properties of tropical soils from TrinidadFront. Microbiol.61045201510.3389/fmicb.2015.01045Search in Google Scholar

Deng L., Zeng G., Fan C., Lu L., Chen X., Chen M., Wu H., He X., He Y.: Response of rhizosphere microbial community structure and diversity to heavy metal co-pollution in arable soil. Appl. Microbiol. Biotechnol. 99, 8259–8269 (2015)DengL.ZengG.FanC.LuL.ChenX.ChenM.WuH.HeX.HeY.Response of rhizosphere microbial community structure and diversity to heavy metal co-pollution in arable soilAppl. Microbiol. Biotechnol.9982598269201510.1007/s00253-015-6662-6Search in Google Scholar

Dunivin T.K., Shade A.: Community structure explains antibiotic resistance gene dynamics over a temperature gradient in soil. FEMS Microbiol. Ecol. 94, fiy016 (2018)DunivinT.K.ShadeA.Community structure explains antibiotic resistance gene dynamics over a temperature gradient in soilFEMS Microbiol. Ecol.94fiy016201810.1093/femsec/fiy016Search in Google Scholar

Fierer N, Schimel J.P.: A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soil. Soil Sci. Soc. Amer. 67, 798–805 (2003)FiererNSchimelJ.P.A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soilSoil Sci. Soc. Amer.67798805200310.2136/sssaj2003.7980Search in Google Scholar

Fierer N, Schimel J.P.: Effects of drying–rewetting frequency on soil carbon and nitrogen transformations. Soil Biol. Biochem. 34, 777–787 (2002)FiererNSchimelJ.P.Effects of drying–rewetting frequency on soil carbon and nitrogen transformationsSoil Biol. Biochem.34777787200210.1016/S0038-0717(02)00007-XSearch in Google Scholar

Fierer N., Jackson R.B.: The diversity and biogeography of soil bacterial communities. PNAS, 103, 3, 626–631 (2006)FiererN.JacksonR.B.The diversity and biogeography of soil bacterial communitiesPNAS1033626631200610.1073/pnas.0507535103133465016407148Search in Google Scholar

Frąc M., Jezierska-Tys S.: Microbial diversity of soil environment. Post. Mikrobiol. 20, 47–58 (2010)FrącM.Jezierska-TysS.Microbial diversity of soil environmentPost. Mikrobiol.2047582010Search in Google Scholar

Fu G., Shen Z.X., Zhang X.X., Zhou Y.T.: Response of soil microbial biomass to short-term experimental warming in alpine meadow on the Tibetan Plateau. Appl. Soil Ecol. 61, 158–160 (2012)FuG.ShenZ.X.ZhangX.X.ZhouY.T.Response of soil microbial biomass to short-term experimental warming in alpine meadow on the Tibetan PlateauAppl. Soil Ecol.61158160201210.1016/j.apsoil.2012.05.002Search in Google Scholar

Gagalidze N.A., Amiranashvili L.L., Sadunishvili T.A., Kvesitadze G.I., Urushadze T.F., Kvrivishvili T.O.: Bacterial composition of different types of soils of Georgia. Ann. Agrar. Sci. 16, 1, 17–27 (2018)GagalidzeN.A.AmiranashviliL.L.SadunishviliT.A.KvesitadzeG.I.UrushadzeT.F.KvrivishviliT.O.Bacterial composition of different types of soils of GeorgiaAnn. Agrar. Sci.1611727201810.1016/j.aasci.2017.08.006Search in Google Scholar

Gałązka A., Łyszcz M., Abramczyk B., Furtak K., Grządziel J., Czaban J., Pikulicka A.: Biodiversity of soil environment – overview of parameters and methods in soil biodiversity analyses. Monografie i rozprawy naukowe IUNG-PIB, Puławy, 2016GałązkaA.ŁyszczM.AbramczykB.FurtakK.GrządzielJ.CzabanJ.PikulickaA.Biodiversity of soil environment – overview of parameters and methods in soil biodiversity analysesMonografie i rozprawy naukowe IUNG-PIBPuławy2016Search in Google Scholar

Gleeson D.B., Herrmann A.M., Livesley S.J, Murphy D.V.: Influence of water potential on nitrification and structure of nitrifying bacterial communities in semiarid soils. Appl. Soil Ecol. 40, 189–194 (2008)GleesonD.B.HerrmannA.M.LivesleyS.JMurphyD.V.Influence of water potential on nitrification and structure of nitrifying bacterial communities in semiarid soilsAppl. Soil Ecol.40189194200810.1016/j.apsoil.2008.02.005Search in Google Scholar

Gliński J., Stępniewska Z., Kasiak A.: Changes of an enzymatic activity in soils with respect to their water content and oxygen status. Roczniki Gleboznawcze, 34, (1–2), 53–59 (1983)GlińskiJ.StępniewskaZ.KasiakA.Changes of an enzymatic activity in soils with respect to their water content and oxygen statusRoczniki Gleboznawcze341–253591983Search in Google Scholar

Gliński J.: Odczyn gleb (in) Gleboznawstwo, Ed. S. Zawadzki, Państwowe Wydawnictwo Rolnicze i Leśne, Warszawa, 1999, p. 220–227GlińskiJ.Odczyn gleb(in)GleboznawstwoEd.ZawadzkiS.Państwowe Wydawnictwo Rolnicze i LeśneWarszawa1999p.220227Search in Google Scholar

Gołębiewski M., Deja-Sikora E., Cichosz M., Tretyn A., Wróbel B.: 16S rDNA Pyrosequencing analysis of bacterial community in heavy metals polluted soils. Microb. Ecol. 67, 3, 635–647 (2014)GołębiewskiM.Deja-SikoraE.CichoszM.TretynA.WróbelB.16S rDNA Pyrosequencing analysis of bacterial community in heavy metals polluted soilsMicrob. Ecol.673635647201410.1007/s00248-013-0344-7396284724402360Search in Google Scholar

Gonet S., Smal H.D., Chojnicki J.: Właściwości chemiczne gleb (in) Gleboznawstwo, Ed. A. Mocek, Wydawnictwo Naukowe PWN, Warszawa, 2015, p. 201–205GonetS.SmalH.D.ChojnickiJ.Właściwości chemiczne gleb(in)GleboznawstwoEd.MocekA.Wydawnictwo Naukowe PWNWarszawa2015p.201205Search in Google Scholar

Gough H.L., Stahl D.A.: Microbial community structures in anoxic freshwater lake sediment along a metal contamination gradient. ISME J. 5 (3), 543–558 (2011)GoughH.L.StahlD.A.Microbial community structures in anoxic freshwater lake sediment along a metal contamination gradientISME J53543558201110.1038/ismej.2010.132310571620811473Search in Google Scholar

Gremion F., Chatzinotas A., Kaufmann K., von Sigler W., Harms H.: Impacts of heavy metal contamination and phytoremediation on a microbial community during a twelve-month microcosm experiment. FEMS Microbiol. Ecol. 48, 2, 273–283 (2004)GremionF.ChatzinotasA.KaufmannK.von SiglerW.HarmsH.Impacts of heavy metal contamination and phytoremediation on a microbial community during a twelve-month microcosm experimentFEMS Microbiol. Ecol.482273283200410.1016/j.femsec.2004.02.00419712410Search in Google Scholar

Grządziel J., Gałązka A.: Microplot long-term experiment reveals strong soil type influence on bacteria composition and its functional diversity. Appl. Soil Ecol. 124, 117–123 (2018)GrządzielJ.GałązkaA.Microplot long-term experiment reveals strong soil type influence on bacteria composition and its functional diversityAppl. Soil Ecol.124117123201810.1016/j.apsoil.2017.10.033Search in Google Scholar

Hallin S., Jones C.M., Schloter M., Philippot L.: Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J. 3, 597–605 (2009)HallinS.JonesC.M.SchloterM.PhilippotL.Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experimentISME J.3597605200910.1038/ismej.2008.12819148144Search in Google Scholar

Hansel C.M., Fendorf S., Jardine P.M., Francis C.A.: Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl. Environ. Microbiol. 74, 1620–1633 (2008)HanselC.M.FendorfS.JardineP.M.FrancisC.A.Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profileAppl. Environ. Microbiol.7416201633200810.1128/AEM.01787-07225862318192411Search in Google Scholar

Henry S., Texier S., Hallet S., Bru D., Dambreville C., Cheneby D., Bizouard F., Germon J.C., Philippot L.: Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudates. Environ. Microbiol. 10, 3082–3092 (2008)HenryS.TexierS.HalletS.BruD.DambrevilleC.ChenebyD.BizouardF.GermonJ.C.PhilippotL.Disentangling the rhizosphere effect on nitrate reducers and denitrifiers: insight into the role of root exudatesEnviron. Microbiol.1030823092200810.1111/j.1462-2920.2008.01599.xSearch in Google Scholar

Hozzein W.N., Li W.J., Ali M.I.A., Hammouda O., Mousa A.S., Xu L.H., Jiang C.L.: Nocardiopsis alkaliphila sp. nov., a novel alkaliphilic actinomycete isolated from desert soil in Egypt. Int. J. Syst. Evol. Microbiol. 54, 247–252 (2004)HozzeinW.N.LiW.J.AliM.I.A.HammoudaO.MousaA.S.XuL.H.JiangC.L.Nocardiopsis alkaliphila sp. nov., a novel alkaliphilic actinomycete isolated from desert soil in EgyptInt. J. Syst. Evol. Microbiol.54247252200410.1099/ijs.0.02832-0Search in Google Scholar

Hus K., Bocian A.: The mechanisms of adaptation allowing bacteria to survive in high temperatures. Kosmos, 66, 2, 175–184 (2017)HusK.BocianA.The mechanisms of adaptation allowing bacteria to survive in high temperaturesKosmos6621751842017Search in Google Scholar

Jayanthi B., Emenike C.U., Agamuthu P., Khanom Simarani, Sharifah Mohamad, Fauziah S.H.: Selected microbial diversity of contaminated landfill soil of Peninsular Malaysia and the behavior towards heavy metal exposure, CATENA, 147, 25–31 (2016)JayanthiB.EmenikeC.U.AgamuthuP.SimaraniKhanomMohamadSharifahFauziahS.H.Selected microbial diversity of contaminated landfill soil of Peninsular Malaysia and the behavior towards heavy metal exposureCATENA1472531201610.1016/j.catena.2016.06.033Search in Google Scholar

Klamkowski K., Treder W., Tryngiel-Gać A., Wójcik K.: Impact of quantity and intensity of precipitation on changes in soil water content in an apple orchard. Infrastructure and Ecology of Rural Areas, 5, 115–126 (2011)KlamkowskiK.TrederW.Tryngiel-GaćA.WójcikK.Impact of quantity and intensity of precipitation on changes in soil water content in an apple orchardInfrastructure and Ecology of Rural Areas51151262011Search in Google Scholar

Kołwzan B., Adamiak W., Grabas K., Pawełczyk A.: Podstawy mikrobiologii w ochronie środowiska. Oficyna Wydawnicza Politechniki Wrocławskiej, Wrocław, 2006KołwzanB.AdamiakW.GrabasK.PawełczykA.Podstawy mikrobiologii w ochronie środowiskaOficyna Wydawnicza Politechniki WrocławskiejWrocław2006Search in Google Scholar

Krebs C.J.: Ecology. The experimental analysis of distribution and abundance. Benjamin Cummings, San Francisco, London, 2001KrebsC.J.Ecology. The experimental analysis of distribution and abundanceBenjamin CummingsSan Francisco, London2001Search in Google Scholar

Krebs C.J.: The Ecological World View. University of California Press, Oakland, 2008, p. 36–38KrebsC.J.The Ecological World ViewUniversity of California PressOakland2008p.363810.1071/9780643098398Search in Google Scholar

Kunicki-Goldfinger W.J.H.: Życie bakterii. Wydawnictwo Naukowe PWN, Warszawa, 2008Kunicki-GoldfingerW.J.H.Życie bakteriiWydawnictwo Naukowe PWNWarszawa2008Search in Google Scholar

Kuramae E.E., Yergeau E., Wong L.C., Pijl A.S., van Veen J.A., Kowalchuk G.A.: Soil characteristics more strongly influence soil bacterial communities than land-use type. FEMS Microbiol. Ecol. 79, 12–24 (2012)KuramaeE.E.YergeauE.WongL.C.PijlA.S.van VeenJ.A.KowalchukG.A.Soil characteristics more strongly influence soil bacterial communities than land-use typeFEMS Microbiol. Ecol.791224201210.1111/j.1574-6941.2011.01192.xSearch in Google Scholar

Ladd J.N., Foster R.C., Nannipieri P., Oades J.: Soil structure and biological activity (in) Soil biochemistry, Ed. G. Stotzky, J.M. Bollag, Vol. 9, Marcel Dekker, New York, 1996, p. 23–78LaddJ.N.FosterR.C.NannipieriP.OadesJ.Soil structure and biological activity(in)Soil biochemistryEd.StotzkyG.BollagJ.M.Vol.9Marcel DekkerNew York1996p.2378Search in Google Scholar

Lee S.H., Sorensen J.W., Grady K.L., Tobin T.C., Shade A.: Divergent extremes but convergent recovery of bacterial and archaeal soil communities to an ongoing subterranean coal mine fire. ISME J. 11 (6), 1447–1459 (2017)LeeS.H.SorensenJ.W.GradyK.L.TobinT.C.ShadeA.Divergent extremes but convergent recovery of bacterial and archaeal soil communities to an ongoing subterranean coal mine fireISME J.11614471459201710.1038/ismej.2017.1Search in Google Scholar

Li G., Kim S., Park M., Son Y.: Short-term effects of experimental warming and precipitation manipulation on soil microbial biomass C and N, community substrate utilization patterns and community composition. Pedosphere, 27, 714–724 (2017)LiG.KimS.ParkM.SonY.Short-term effects of experimental warming and precipitation manipulation on soil microbial biomass C and N, community substrate utilization patterns and community compositionPedosphere27714724201710.1016/S1002-0160(17)60408-9Search in Google Scholar

Li X., Meng D., Li J., Yin H., Liu H., Liu X., Cheng C., Xiao Y., Liu Z. Yan M.: Response of soil microbial communities and microbial interactions to long-term heavy metal contamination. Environ. Pollut. 231, 908–917 (2017)LiX.MengD.LiJ.YinH.LiuH.LiuX.ChengC.XiaoY.LiuZ. Yan M.Response of soil microbial communities and microbial interactions to long-term heavy metal contaminationEnviron. Pollut.231908917201710.1016/j.envpol.2017.08.05728886536Search in Google Scholar

Libudzisz Z., Kowal K., Żakowska Z.: Mikrobiologia techniczna. Wydawnictwo Naukowe PWN, Warszawa, 2007LibudziszZ.KowalK.ŻakowskaZ.Mikrobiologia technicznaWydawnictwo Naukowe PWNWarszawa2007Search in Google Scholar

Lozupone C.A., Knight R.: Global patterns in bacterial diversity. PNAS, 104, 11436–11440 (2007)LozuponeC.A.KnightR.Global patterns in bacterial diversityPNAS1041143611440200710.1073/pnas.0611525104204091617592124Search in Google Scholar

Lynch M., Gabriel W.: Environmental Tolerance. Am. Nat. 129, 2, 283–303 (1987)LynchM.GabrielW.Environmental ToleranceAm. Nat1292283303198710.1086/284635Search in Google Scholar

Maranguit D., Guillaume T., Kuzyakov Y.: Effects of flooding on phosphorus and iron mobilization in highly weathered soils under different land-use types: Short-term effects and mechanisms. CATENA, 158, 161–170 (2017)MaranguitD.GuillaumeT.KuzyakovY.Effects of flooding on phosphorus and iron mobilization in highly weathered soils under different land-use types: Short-term effects and mechanismsCATENA158161170201710.1016/j.catena.2017.06.023Search in Google Scholar

Marschner P., Yang C.H., Lieberei R., Crowley D.: Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol. Biochem. 33, 1437–1445 (2001)MarschnerP.YangC.H.LiebereiR.CrowleyD.Soil and plant specific effects on bacterial community composition in the rhizosphereSoil Biol. Biochem.3314371445200110.1016/S0038-0717(01)00052-9Search in Google Scholar

Marshall P.F.: Induced plant defenses against pathogens and herbivores: biochemistry, ecology, and agriculture. APS Press, St. Paul, 1997MarshallP.F.Induced plant defenses against pathogens and herbivores: biochemistry, ecology, and agricultureAPS PressSt. Paul1997Search in Google Scholar

Mazur Z., Mazur T.: Organic carbon content and its fractions in soils of multi-year fertilization experiments. Pol. J. Environ. Stud. 24, 4, 1697–1703 (2015)MazurZ.MazurT.Organic carbon content and its fractions in soils of multi-year fertilization experimentsPol. J. Environ. Stud.24416971703201510.15244/pjoes/31687Search in Google Scholar

Meliani A., Bensoltane A., Mederbel K.: Microbial diversity and abundance in soil: related to plant and soil type. Am. J. Plant Nutr. Fert. Techno. 2, 10–18 (2012)MelianiA.BensoltaneA.MederbelK.Microbial diversity and abundance in soil: related to plant and soil typeAm. J. Plant Nutr. Fert. Techno.21018201210.3923/ajpnft.2012.10.18Search in Google Scholar

Mhuantong W., Champreda V. et al.: Survey of Microbial Diversity in Flood Areas during Thailand 2011 Flood Crisis Using High-Throughput Tagged Amplicon Pyrosequencing. Plos One, 10, e0128043 (2015)MhuantongW.ChampredaV.Survey of Microbial Diversity in Flood Areas during Thailand 2011 Flood Crisis Using High-Throughput Tagged Amplicon PyrosequencingPlos One10e0128043201510.1371/journal.pone.0128043444736426020967Search in Google Scholar

Mohammed U.A., Zigau Z.A.: Influence of soil pH and temperature on soil microflora. Gashua J. Sci. Hum. 2, 39–47 (2016)MohammedU.A.ZigauZ.A.Influence of soil pH and temperature on soil microfloraGashua J. Sci. Hum.239472016Search in Google Scholar

Nannipieri P., Ascher J., Ceccherini M.T., Landi L., Pietramellara G., Renella G.: Microbial diversity and soil functions. Eur. J. Soil Sci. 54, 655–670 (2003)NannipieriP.AscherJ.CeccheriniM.T.LandiL.PietramellaraG.RenellaG.Microbial diversity and soil functionsEur. J. Soil Sci.54655670200310.1046/j.1351-0754.2003.0556.xSearch in Google Scholar

Niemczyk H., Kowalska B., Majewski G.: The formation of actual soil moisture depending on the amount of precipitation and air temperature. Przegląd Naukowy Inżynieria i Kształtowanie Środowiska, 2 (36), 11–19 (2007)NiemczykH.KowalskaB.MajewskiG.The formation of actual soil moisture depending on the amount of precipitation and air temperaturePrzegląd Naukowy Inżynieria i Kształtowanie Środowiska23611192007Search in Google Scholar

Pariona-Llanos R., Ibañez de Santi Ferrara F., Soto-Gonzales H.H., Barbosa H.R.: Influence of organic fertilization on the number of culturable diazotrophic endophytic bacteria isolated from sugarcane. Eur. J. Soil Biol. 46, 387–393 (2010)Pariona-LlanosR.Ibañez de Santi FerraraF.Soto-GonzalesH.H.BarbosaH.R.Influence of organic fertilization on the number of culturable diazotrophic endophytic bacteria isolated from sugarcaneEur. J. Soil Biol.46387393201010.1016/j.ejsobi.2010.08.003Search in Google Scholar

Pascual I., Antolin M.C., Garcia C., Polo A., Sanchez-Diaz M.: Effect of water deficit on microbial characteristics in soil amended with sewage sludge or inorganic fertilizer under laboratory conditions. Biores. Technol. 98, 29–37 (2007)PascualI.AntolinM.C.GarciaC.PoloA.Sanchez-DiazM.Effect of water deficit on microbial characteristics in soil amended with sewage sludge or inorganic fertilizer under laboratory conditionsBiores. Technol.982937200710.1016/j.biortech.2005.11.02616427275Search in Google Scholar

Qi D., Wieneke X., Tao J., Zhou X., Desilva U.: Soil pH is the primary factor correlating with soil microbiome in karst rocky desertification regions in the Wushan County, Chongqing, China. Front. Microbiol. 9, 1027 (2018)QiD.WienekeX.TaoJ.ZhouX.DesilvaU.Soil pH is the primary factor correlating with soil microbiome in karst rocky desertification regions in the Wushan County, Chongqing, ChinaFront. Microbiol.91027201810.3389/fmicb.2018.01027598775729896164Search in Google Scholar

Ramirez K.S., Lauber C.L., Knight R., Bradford M.A., Fierer N.: Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems. Ecology, 91, 3463–3470 (2010)RamirezK.S.LauberC.L.KnightR.BradfordM.A.FiererN.Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systemsEcology9134633470201010.1890/10-0426.121302816Search in Google Scholar

Rampelotto P.H.: Resistance of microorganisms to extreme environmental conditions and its contribution to astrobiology. Sustainability, 2, 1602–1623 (2010)RampelottoP.H.Resistance of microorganisms to extreme environmental conditions and its contribution to astrobiologySustainability216021623201010.3390/su2061602Search in Google Scholar

Rietz D.N., Haynes R.J.: Effects of irrigation-induced salinity and sodicity on soil microbial activity. Soil Biol. Biochem. 35, 845–854 (2003)RietzD.N.HaynesR.J.Effects of irrigation-induced salinity and sodicity on soil microbial activitySoil Biol. Biochem.35845854200310.1016/S0038-0717(03)00125-1Search in Google Scholar

Rojek E., Usowicz B.: Spatial variability of soil temperature in Poland. Acta Agroph. 25, 289–305 (2018)RojekE.UsowiczB.Spatial variability of soil temperature in PolandActa Agroph.25289305201810.31545/aagr/95026Search in Google Scholar

Rousk J., Brookes P.C., Bååth E.: Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl. Environ. Microb. 75, 1589–1596 (2009)RouskJ.BrookesP.C.BååthE.Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralizationAppl. Environ. Microb.7515891596200910.1128/AEM.02775-08265547519151179Search in Google Scholar

Rousseau S., Doneche B.: Effects of water activity (aw) on the growth of some epiphytic microorganisms isolated from grape berry. Vitis. 40, 75–78 (2001)RousseauS.DonecheB.Effects of water activity (aw) on the growth of some epiphytic microorganisms isolated from grape berryVitis.4075782001Search in Google Scholar

Schneider A.R., Marin B. et al.: Response of bacterial communities to Pb smelter pollution in contrasting soils. Sci. Total Environ. 605–606, 436–444 (2017)SchneiderA.R.MarinB.Response of bacterial communities to Pb smelter pollution in contrasting soilsSci. Total Environ.605–606436444201710.1016/j.scitotenv.2017.06.15928672232Search in Google Scholar

Schreiter S., Ding G.C., Heuer H., Neumann G., Sandmann M., Grosch R., Kropf S., Smalla K.: Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front. Microbiol. 5, 144 (2014)SchreiterS.DingG.C.HeuerH.NeumannG.SandmannM.GroschR.KropfS.SmallaK.Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuceFront. Microbiol.5144201410.3389/fmicb.2014.00144398652724782839Search in Google Scholar

Sessitsch A., Weilharter A., Gerzabek M.H., Kirchmann H., Kandeler E.: Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment. Appl. Environ. Microb. 67, 4215–24 (2001)SessitschA.WeilharterA.GerzabekM.H.KirchmannH.KandelerE.Microbial population structures in soil particle size fractions of a long-term fertilizer field experimentAppl. Environ. Microb.67421524200110.1128/AEM.67.9.4215-4224.20019315011526026Search in Google Scholar

Sheik C.S., Mitchell T.W., Rizvi F.Z., Rehman Y., Faisal M., Hasnain S., McInerney M.J., Krumholz L.R.: Exposure of soil microbial communities to chromium and arsenic alters their diversity and structure. Plos ONE, 7, e40059 (2012)SheikC.S.MitchellT.W.RizviF.Z.RehmanY.FaisalM.HasnainS.McInerneyM.J.KrumholzL.R.Exposure of soil microbial communities to chromium and arsenic alters their diversity and structurePlos ONE7e40059201210.1371/journal.pone.0040059338695022768219Search in Google Scholar

Shukla L., Suman A., Yadav A.N., Verma P., Saxena A.K.: Syntrophic microbial system for ex-situ degradation of paddy straw at low temperature under controlled and natural environment. J. Appl. Biol. Biotechnol. 4 (2), 30–37 (2016)ShuklaL.SumanA.YadavA.N.VermaP.SaxenaA.K.Syntrophic microbial system for ex-situ degradation of paddy straw at low temperature under controlled and natural environmentJ. Appl. Biol. Biotechnol.4230372016Search in Google Scholar

Sochocka M., Boratyński J.: Osmoregulation – an important parameter of bacterial growth. Postępy Higieny i Medycyny Doświadczalnej, 65, 714–724 (2011)SochockaM.BoratyńskiJ.Osmoregulation – an important parameter of bacterial growthPostępy Higieny i Medycyny Doświadczalnej65714724201110.5604/17322693.96660422173436Search in Google Scholar

Staszewski Z.: Nitrogen in soil and its impact upon environment. Zeszyty Naukowe. Inżynieria Lądowa i Wodna w Kształtowaniu Środowiska, 4, 50–58 (2011)StaszewskiZ.Nitrogen in soil and its impact upon environmentZeszyty Naukowe. Inżynieria Lądowa i Wodna w Kształtowaniu Środowiska450582011Search in Google Scholar

Tipayno S., Truu J., Samaddar S., Truu M., Preem J., Oopkaup K., Espenberg M., Chattarjee P., Kang Y., Kim K., Sa T.: The bacterial community structure and functional profile in the heavy metal contaminated paddy soils, surrounding a nonferrous smelter in South Korea. Ecol. Evol. 8, 12, 6157–6168 (2018)TipaynoS.TruuJ.SamaddarS.TruuM.PreemJ.OopkaupK.EspenbergM.ChattarjeeP.KangY.KimK.SaT.The bacterial community structure and functional profile in the heavy metal contaminated paddy soils, surrounding a nonferrous smelter in South KoreaEcol. Evol.81261576168201810.1002/ece3.4170602415029988438Search in Google Scholar

Unger I.M., Kennedy A.C., Muzika R.M., 2009. Flooding effects on soil microbial communities. Appl. Soil Ecol. 42 (1): 1–8.UngerI.M.KennedyA.C.MuzikaR.M.2009Flooding effects on soil microbial communitiesAppl. Soil Ecol.4211810.1016/j.apsoil.2009.01.007Search in Google Scholar

Wagner D., Eisenhauer N., Cesarz S.: Plant species richness does not attenuate responses of soil microbial and nematode communities to a flood event. Soil Biol. Biochem. 89, 135–149 (2015)WagnerD.EisenhauerN.CesarzS.Plant species richness does not attenuate responses of soil microbial and nematode communities to a flood eventSoil Biol. Biochem.89135149201510.1016/j.soilbio.2015.07.001Search in Google Scholar

Wichern J., Wichern F., Joergensen R.G.: Impact of salinity on soil microbial communities and the decomposition of maize in acidic soils. Geoderma, 137, 100–108 (2006)WichernJ.WichernF.JoergensenR.G.Impact of salinity on soil microbial communities and the decomposition of maize in acidic soilsGeoderma137100108200610.1016/j.geoderma.2006.08.001Search in Google Scholar

Wolińska A.: Dehydrogenases activity of soil microorganisms and oxygen availability during reoxidation process of selected mineral soils from Poland. Acta Agrophys. Rozprawy i monografie. 180 (3), 5–87 (2010)WolińskaA.Dehydrogenases activity of soil microorganisms and oxygen availability during reoxidation process of selected mineral soils from Poland. Acta AgrophysRozprawy i monografie18035872010Search in Google Scholar

Wolińska A.: Metagenomic achievements in microbial diversity determination in croplands: a review (in) Microbial Diversity in Genomic Era, Ed. S. Das, H.R. Dash, Academic Press Elsevier, The Netherlands, Amsterdam, 2019, p. 15–35WolińskaA.Metagenomic achievements in microbial diversity determination in croplands: a review(in)Microbial Diversity in Genomic EraEd.DasS.DashH.R.Academic Press ElsevierThe Netherlands, Amsterdam2019p.153510.1016/B978-0-12-814849-5.00002-2Search in Google Scholar

Yadav A.N., Verma P., Sachan S.G., Kaushik R., Saxena A.K.: Psychrotrophic microbiomes: molecular diversity and beneficial role in plant growth promotion and soil health (in) Microorganisms for green revolution: microbes for sustainable agro-ecosystem, Ed. D.G. Panpatte, Y.K. Jhala, H.N. Shelat, R.V. Vyas, Vol. 2, Springer, Singapore, 2018, p. 197–240YadavA.N.VermaP.SachanS.G.KaushikR.SaxenaA.K.Psychrotrophic microbiomes: molecular diversity and beneficial role in plant growth promotion and soil health(in)Microorganisms for green revolution: microbes for sustainable agro-ecosystemEd.PanpatteD.G.JhalaY.K.ShelatH.N.VyasR.V.Vol.2SpringerSingapore2018p.19724010.1007/978-981-10-7146-1_11Search in Google Scholar

Yan N., Marschner P., Cao W., Zuo C., Qin W.: Influence of salinity and water content on soil microorganisms. International Soil and Water Conservation Research, 3, 316–323 (2015)YanN.MarschnerP.CaoW.ZuoC.QinW.Influence of salinity and water content on soil microorganismsInternational Soil and Water Conservation Research3316323201510.1016/j.iswcr.2015.11.003Search in Google Scholar

Young I.M., Ritz K.: Tillage, habitat space and function of soil microbes. Soil Till. Res. 53, 201–213 (2000)YoungI.M.RitzK.Tillage, habitat space and function of soil microbesSoil Till. Res.53201213200010.1016/S0167-1987(99)00106-3Search in Google Scholar

Zhang W., Parker K.M., Luo Y., Wan S., Wallace L.L., Hu S.: Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Glob. Change Biol. 11, 266–277 (2005)ZhangW.ParkerK.M.LuoY.WanS.WallaceL.L.HuS.Soil microbial responses to experimental warming and clipping in a tallgrass prairieGlob. Change Biol.11266277200510.1111/j.1365-2486.2005.00902.xSearch in Google Scholar

Zhang Y., Shen H., He X., Thomas B.W., Lupywayi N.Z., Hao X., Thomas M.C., Shi X.: Fertilization shapes bacterial community structure by alteration of soil pH. Front. Microbiol. 8, 1325 (2017)ZhangY.ShenH.HeX.ThomasB.W.LupywayiN.Z.HaoX.ThomasM.C.ShiX.Fertilization shapes bacterial community structure by alteration of soil pHFront. Microbiol.81325201710.3389/fmicb.2017.01325551396928769896Search in Google Scholar

Zhou J., Xia B., Treves D.S., Wu L.Y., Marsh T.L., O’Neill R.V., Palumbo A.V., Tiedje J.M.: Spatial and resource factors influencing high microbial diversity in soil. Appl. Environ. Microbiol. 68, 326–334 (2002)ZhouJ.XiaB.TrevesD.S.WuL.Y.MarshT.L.O’NeillR.V.PalumboA.V.TiedjeJ.M.Spatial and resource factors influencing high microbial diversity in soilAppl. Environ. Microbiol.68326334200210.1128/AEM.68.1.326-334.200212656411772642Search in Google Scholar

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