Isolation, Identification, and Fermentation Medium Optimization of a Caproic Acid‑Producing Enterococcus casseliflavus Strain from Pit Mud of Chinese Strong Flavor Baijiu Ecosystem

Akbari H, Shekrabi SPH, Soltani M, Mehrgan MS. Effects of potential probiotic Enterococcus casseliflavus (EC-001) on growth performance, immunity, and resistance to Aeromonas hydrophila infection in common carp (Cyprinus carpio). Probiotics Antimicrob Proteins. 2021 Oct;13(5):1316–1325. https://doi.org/10.1007/s12602-021-09771-xAkbari H Shekrabi SPH Soltani M Mehrgan MS Effects of potential probiotic Enterococcus casseliflavus (EC-001) on growth performance, immunity, and resistance to Aeromonas hydrophila infection in common carp (Cyprinus carpio) Probiotics Antimicrob Proteins 2021 Oct1351316 1325 https://doi.org/10.1007/s12602-021-09771-x10.1007/s12602-021-09771-x33721202Search in Google Scholar

Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012 May;19(5):455–477. https://doi.org/10.1089/cmb.2012.0021Bankevich A Nurk S Antipov D Gurevich AA Dvorkin M Kulikov AS Lesin VM Nikolenko SI Pham S Prjibelski AD et al SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing J Comput Biol 2012 May195455 477 https://doi.org/10.1089/cmb.2012.002110.1089/cmb.2012.0021334251922506599Search in Google Scholar

Blake JD, Cohen FE. Pairwise sequence alignment below the twilight zone. J Mol Biol. 2001 Mar 23;307(2):721–735. https://doi.org/10.1006/jmbi.2001.4495Blake JD Cohen FE Pairwise sequence alignment below the twilight zone J Mol Biol 2001 Mar 233072721 735 https://doi.org/10.1006/jmbi.2001.449510.1006/jmbi.2001.449511254392Search in Google Scholar

Ceddia T, Mancini A, Marinucci MC. [A new ICSB classification of Staphylococci stocks previously classified according to Bergey’s Manual of Determinative Bacteriology] (in Italian). Boll Soc Ital Biol Sper. 1980 Jul 15;56(13):1409–1413.Ceddia T Mancini A Marinucci MC [A new ICSB classification of Staphylococci stocks previously classified according to Bergey’s Manual of Determinative Bacteriology] (in Italian) Boll Soc Ital Biol Sper 1980 Jul 1556131409 1413Search in Google Scholar

Christ JJ, Blank LM. Saccharomyces cerevisiae containing 28% polyphosphate and production of a polyphosphate-rich yeast extract thereof. FEMS Yeast Res. 2019 May 1;19(3):foz011. https://doi.org/10.1093/femsyr/foz011Christ JJ Blank LM Saccharomyces cerevisiae containing 28% polyphosphate and production of a polyphosphate-rich yeast extract thereof FEMS Yeast Res 2019 May 1193foz011 https://doi.org/10.1093/femsyr/foz01110.1093/femsyr/foz01130721988Search in Google Scholar

Coil D, Jospin G, Darling AE. A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics. 2015 Feb 15;31(4):587–589. https://doi.org/10.1093/bioinformatics/btu661Coil D Jospin G Darling AE A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data Bioinformatics 2015 Feb 15314587 589 https://doi.org/10.1093/bioinformatics/btu66110.1093/bioinformatics/btu66125338718Search in Google Scholar

Dobritsa AP, Kutumbaka KK, Werner K, Wiedmann M, Asmus A, Samadpour M. Clostridium tepidum sp. nov., a close relative of Clostridium sporogenes and Clostridium botulinum Group I. Int J Syst Evol Microbiol. 2017 Jul;67(7):2317–2322. https://doi.org/10.1099/ijsem.0.001948Dobritsa AP Kutumbaka KK Werner K Wiedmann M Asmus A Samadpour M Clostridium tepidum sp nov., a close relative of Clostridium sporogenes and Clostridium botulinum Group I. Int J Syst Evol Microbiol 2017 Jul6772317 2322 https://doi.org/10.1099/ijsem.0.00194810.1099/ijsem.0.00194828693684Search in Google Scholar

Gildemyn S, Molitor B, Usack JG, Nguyen M, Rabaey K, Angenent LT. Upgrading syngas fermentation effluent using Clostridium kluyveri in a continuous fermentation. Biotechnol Biofuels. 2017 Mar 29;10:83. https://doi.org/10.1186/s13068-017-0764-6Gildemyn S Molitor B Usack JG Nguyen M Rabaey K Angenent LT Upgrading syngas fermentation effluent using Clostridium kluyveri in a continuous fermentation Biotechnol Biofuels 2017 Mar 291083 https://doi.org/10.1186/s13068-017-0764-610.1186/s13068-017-0764-6537233128367228Search in Google Scholar

Gou WJ, Tian Y, Kong XY, Wu FF, Fang F. [Bacterial composition in pit mud of Yanghe liquor and identification of acid producing bacteria] (in Chinese). Microbiol. China. 2020 Jun:47(6):1651–1661. https://doi.org/10.13344/j.microbiol.china.190839Gou WJ Tian Y Kong XY Wu FF Fang F [Bacterial composition in pit mud of Yanghe liquor and identification of acid producing bacteria] (in Chinese) Microbiol. China 2020 Jun4761651 1661 https://doi.org/10.13344/j.microbiol.china.190839Search in Google Scholar

Hong J, Tian W, Zhao D. Research progress of trace components in sesame-aroma type of baijiu. Food Res Int. 2020 Nov;137:109695. https://doi.org/10.1016/j.foodres.2020.109695Hong J Tian W Zhao D Research progress of trace components in sesame-aroma type of baijiu Food Res Int 2020 Nov137109695 https://doi.org/10.1016/j.foodres.2020.10969510.1016/j.foodres.2020.10969533233269Search in Google Scholar

Hu XL, Du H, Xu Y. Identification and quantification of the caproic acid-producing bacterium Clostridium kluyveri in the fermentation of pit mud used for Chinese strong-aroma type liquor production. Int J Food Microbiol. 2015 Dec 2;214:116–122. https://doi.org/10.1016/j.ijfoodmicro.2015.07.032Hu XL Du H Xu Y Identification and quantification of the caproic acid-producing bacterium Clostridium kluyveri in the fermentation of pit mud used for Chinese strong-aroma type liquor production Int J Food Microbiol 2015 Dec 2214116 122 https://doi.org/10.1016/j.ijfoodmicro.2015.07.03210.1016/j.ijfoodmicro.2015.07.03226267890Search in Google Scholar

Ji X, Xu Y, Mu XQ, Ge XY. [Improvement of caproic acid production in the mixed culture of Clostridium kluyveri and Saccharomyces cerevisiae] (in Chinese). J Food Sci Biotechnol. 2017 Sep; 36(09): 922–926.Ji X Xu Y Mu XQ Ge XY [Improvement of caproic acid production in the mixed culture of Clostridium kluyveri and Saccharomyces cerevisiae] (in Chinese) J Food Sci Biotechnol 2017 Sep 3609 922 926Search in Google Scholar

Kalvari I, Argasinska J, Quinones-Olvera N, Nawrocki EP, Rivas E, Eddy SR, Bateman A, Finn RD, Petrov AI. Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families. Nucleic Acids Res. 2018 Jan 4;46(D1):D335–D342. https://doi.org/10.1093/nar/gkx1038Kalvari I Argasinska J Quinones-Olvera N Nawrocki EP Rivas E Eddy SR Bateman A Finn RD Petrov AI Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families Nucleic Acids Res 2018 Jan 446D1D335 D342 https://doi.org/10.1093/nar/gkx103810.1093/nar/gkx1038575334829112718Search in Google Scholar

Kim BC, Seung Jeon B, Kim S, Kim H, Um Y, Sang BI. Caproiciproducens galactitolivorans gen. nov., sp. nov., a bacterium capable of producing caproic acid from galactitol, isolated from a wastewater treatment plant. Int J Syst Evol Microbiol. 2015 Dec; 65(Pt_12): 4902–4908. https://doi.org/10.1099/ijsem.0.000665Kim BC Seung Jeon B Kim S Kim H Um Y Sang BI Caproiciproducens galactitolivorans gen nov., sp. nov., a bacterium capable of producing caproic acid from galactitol, isolated from a wastewater treatment plant. Int J Syst Evol Microbiol 2015 Dec 65Pt_12 4902 4908 https://doi.org/10.1099/ijsem.0.00066510.1099/ijsem.0.00066526474980Search in Google Scholar

Kim H, Jeon BS, Pandey A, Sang BI. New coculture system of Clostridium spp. and Megasphaera hexanoica using submerged hollow-fiber membrane bioreactors for caproic acid production. Bioresour Technol. 2018 Dec;270:498–503. https://doi.org/10.1016/j.biortech.2018.09.033Kim H Jeon BS Pandey A Sang BI New coculture system of Clostridium spp and Megasphaera hexanoica using submerged hollow-fiber membrane bioreactors for caproic acid production. Bioresour Technol 2018 Dec270498 503 https://doi.org/10.1016/j.biortech.2018.09.03310.1016/j.biortech.2018.09.03330245320Search in Google Scholar

Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Mol Biol Evol. 2016 Jul;33(7):1870–1874. https://doi.org/10.1093/molbev/msw054Kumar S Stecher G Tamura K MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets Mol Biol Evol 2016 Jul3371870 1874 https://doi.org/10.1093/molbev/msw05410.1093/molbev/msw054821082327004904Search in Google Scholar

Liu H, Sun B. Effect of fermentation processing on the flavor of baijiu. J Agric Food Chem. 2018 Jun 6;66(22):5425–5432. https://doi.org/10.1021/acs.jafc.8b00692Liu H Sun B Effect of fermentation processing on the flavor of baijiu J Agric Food Chem 2018 Jun 666225425 5432 https://doi.org/10.1021/acs.jafc.8b0069210.1021/acs.jafc.8b0069229751730Search in Google Scholar

Lowe TM, Eddy SR. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997 Mar 1;25(5):955–964. https://doi.org/10.1093/nar/25.5.955Lowe TM Eddy SR tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence Nucleic Acids Res 1997 Mar 1255955 964 https://doi.org/10.1093/nar/25.5.95510.1093/nar/25.5.9551465259023104Search in Google Scholar

Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007 Jul;35(Suppl_2):W182–W185. https://doi.org/10.1093/nar/gkm321Moriya Y Itoh M Okuda S Yoshizawa AC Kanehisa M KAAS: an automatic genome annotation and pathway reconstruction server Nucleic Acids Res 2007 Jul35Suppl_2W182 W185 https://doi.org/10.1093/nar/gkm32110.1093/nar/gkm321193319317526522Search in Google Scholar

Nabi MN, Akhter MS, Zaglul Shahadat MM. Improvement of engine emissions with conventional diesel fuel and diesel-biodiesel blends. Bioresour Technol. 2006 Feb;97(3):372–378. https://doi.org/10.1016/j.biortech.2005.03.013Nabi MN Akhter MS Zaglul Shahadat MM Improvement of engine emissions with conventional diesel fuel and diesel-biodiesel blends Bioresour Technol 2006 Feb973372 378 https://doi.org/10.1016/j.biortech.2005.03.01310.1016/j.biortech.2005.03.01315905086Search in Google Scholar

Qin X, Galloway-Peña JR, Sillanpaa J, Roh JH, Nallapareddy SR, Chowdhury S, Bourgogne A, Choudhury T, Muzny DM, Buhay CJ, et al. Complete genome sequence of Enterococcus faecium strain TX16 and comparative genomic analysis of Enterococcus faecium genomes. BMC Microbiol. 2012 Jul 7;12:135. https://doi.org/10.1186/1471-2180-12-135Qin X Galloway-Peña JR Sillanpaa J Roh JH Nallapareddy SR Chowdhury S Bourgogne A Choudhury T Muzny DM Buhay CJ et al Complete genome sequence of Enterococcus faecium strain TX16 and comparative genomic analysis of Enterococcus faecium genomes BMC Microbiol 2012 Jul 712135 https://doi.org/10.1186/1471-2180-12-13510.1186/1471-2180-12-135343335722769602Search in Google Scholar

Serhan M, Mattar J, Debs L. Concentrated yogurt (Labneh) made of a mixture of goats’ and cows’ milk: physicochemical, microbiological and sensory analysis. Small Rumin Res. 2016 May;138:46–52. https://doi.org/10.1016/j.smallrumres.2016.04.003Serhan M Mattar J Debs L Concentrated yogurt (Labneh) made of a mixture of goats’ and cows’ milk: physicochemical, microbiological and sensory analysis Small Rumin Res 2016 May13846 52 https://doi.org/10.1016/j.smallrumres.2016.04.00310.1016/j.smallrumres.2016.04.003Search in Google Scholar

Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019 Jan 8;47(D1):D607–D613. https://doi.org/10.1093/nar/gky1131Szklarczyk D Gable AL Lyon D Junge A Wyder S Huerta-Cepas J Simonovic M Doncheva NT Morris JH Bork P et al STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets Nucleic Acids Res 2019 Jan 847D1D607 D613 https://doi.org/10.1093/nar/gky113110.1093/nar/gky1131632398630476243Search in Google Scholar

Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Lomsadze A, Pruitt KD, Borodovsky M, Ostell J. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016 Aug 19;44(14):6614–6624. https://doi.org/10.1093/nar/gkw569Tatusova T DiCuccio M Badretdin A Chetvernin V Nawrocki EP Zaslavsky L Lomsadze A Pruitt KD Borodovsky M Ostell J NCBI prokaryotic genome annotation pipeline Nucleic Acids Res 2016 Aug 1944146614 6624 https://doi.org/10.1093/nar/gkw56910.1093/nar/gkw569500161127342282Search in Google Scholar

Thurlow LR, Thomas VC, Fleming SD, Hancock LE. Enterococcus faecalis capsular polysaccharide serotypes C and D and their contributions to host innate immune evasion. Infect Immun. 2009 Dec; 77(12):5551–5557. https://doi.org/10.1128/IAI.00576-09Thurlow LR Thomas VC Fleming SD Hancock LE Enterococcus faecalis capsular polysaccharide serotypes C and D and their contributions to host innate immune evasion Infect Immun 2009 Dec 77125551 5557 https://doi.org/10.1128/IAI.00576-0910.1128/IAI.00576-09278647119805541Search in Google Scholar

Tian N, Guo X, Wang M, Chen C, Cui H, Zhang L, Tang H. Bacterial community diversity of shilixiang baijiu Daqu based on metagenomics. J Food Biochem. 2020 Jul 29:e13410. https://doi.org/10.1111/jfbc.13410Tian N Guo X Wang M Chen C Cui H Zhang L Tang H Bacterial community diversity of shilixiang baijiu Daqu based on metagenomics J Food Biochem 2020 Jul 29e13410 https://doi.org/10.1111/jfbc.1341010.1111/jfbc.1341032729122Search in Google Scholar

Van Immerseel F, De Buck J, Boyen F, Bohez L, Pasmans F, Volf J, Sevcik M, Rychlik I, Haesebrouck F, Ducatelle R. Medium-chain fatty acids decrease colonization and invasion through hilA suppression shortly after infection of chickens with Salmonella enterica serovar Enteritidis. Appl Environ Microbiol. 2004 Jun;70(6):3582–3587. https://doi.org/10.1128/AEM.70.6.3582-3587.2004Van Immerseel F De Buck J Boyen F Bohez L Pasmans F Volf J Sevcik M Rychlik I Haesebrouck F Ducatelle R Medium-chain fatty acids decrease colonization and invasion through hilA suppression shortly after infection of chickens with Salmonella enterica serovar Enteritidis Appl Environ Microbiol 2004 Jun7063582 3587 https://doi.org/10.1128/AEM.70.6.3582-3587.200410.1128/AEM.70.6.3582-3587.200442775715184160Search in Google Scholar

Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, et al. Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014 Nov 19;9(11): e112963. https://doi.org/10.1371/journal.pone.0112963Walker BJ Abeel T Shea T Priest M Abouelliel A Sakthikumar S Cuomo CA Zeng Q Wortman J Young SK et al Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement PLoS One 2014 Nov 19911 e112963 https://doi.org/10.1371/journal.pone.011296310.1371/journal.pone.0112963423734825409509Search in Google Scholar

Wang MY, Yang JG, Zhao QS, Zhang KZ, Su C. Research progress on flavor compounds and microorganisms of Maotai flavor baijiu. J Food Sci. 2019 Jan;84(1):6–18. https://doi.org/10.1111/1750-3841.14409Wang MY Yang JG Zhao QS Zhang KZ Su C Research progress on flavor compounds and microorganisms of Maotai flavor baijiu J Food Sci 2019 Jan8416 18 https://doi.org/10.1111/1750-3841.1440910.1111/1750-3841.1440930548499Search in Google Scholar

Wang Q, Zhang P, Bao S, Liang J, Wu Y, Chen N, Wang S, Cai Y. Chain elongation performances with anaerobic fermentation liquid from sewage sludge with high total solid as electron acceptor. Bioresour Technol. 2020 Mar 14;306:123188. https://doi.org/10.1016/j.biortech.2020.123188Wang Q Zhang P Bao S Liang J Wu Y Chen N Wang S Cai Y Chain elongation performances with anaerobic fermentation liquid from sewage sludge with high total solid as electron acceptor Bioresour Technol 2020 Mar 14306123188 https://doi.org/10.1016/j.biortech.2020.12318810.1016/j.biortech.2020.12318832199398Search in Google Scholar

Weimer PJ, Stevenson DM. Isolation, characterization, and quantification of Clostridium kluyveri from the bovine rumen. Appl Microbiol Biotechnol. 2012 Apr;94(2):461–466. https://doi.org/10.1007/s00253-011-3751-zWeimer PJ Stevenson DM Isolation, characterization, and quantification of Clostridium kluyveri from the bovine rumen Appl Microbiol Biotechnol 2012 Apr942461 466 https://doi.org/10.1007/s00253-011-3751-z10.1007/s00253-011-3751-z22159841Search in Google Scholar

Yuan S, Jin Z, Ali A, Wang C, Liu J. Caproic acid-producing bacteria in Chinese Baijiu Brewing. Front Microbiol. 2022 May 4; 13:883142. https://doi.org/10.3389/fmicb.2022.883142Yuan S Jin Z Ali A Wang C Liu J Caproic acid-producing bacteria in Chinese Baijiu Brewing Front Microbiol 2022 May 4 13883142 https://doi.org/10.3389/fmicb.2022.88314210.3389/fmicb.2022.883142911450835602080Search in Google Scholar

Zhao H, Chang Y, Wang W, Ling HZ, Ping WX, Zhao ZC, Yang ZH. [Isolation and identification of facultative anaerobic strains with high yield of hexanoic acid from Luzhou-flavor liquor pit mud] (in Chinese). Food Sci. 2012 Sep;33(05):177–182.Zhao H Chang Y Wang W Ling HZ Ping WX Zhao ZC Yang ZH [Isolation and identification of facultative anaerobic strains with high yield of hexanoic acid from Luzhou-flavor liquor pit mud] (in Chinese) Food Sci 2012 Sep3305177 182Search in Google Scholar

Zhao T, Ni D, Hu G, Wang L, Chen S, Xu Y. 6-(2-Formyl-5-methyl-1H-pyrrol-1-yl)hexanoic acid as a novel retronasal burnt aroma compound in soy sauce aroma-type Chinese Baijiu. J Agric Food Chem. 2019 Jul 17;67(28):7916–7925. https://doi.org/10.1021/acs.jafc.9b02095Zhao T Ni D Hu G Wang L Chen S Xu Y 6-(2-Formyl-5-methyl-1H-pyrrol-1-yl)hexanoic acid as a novel retronasal burnt aroma compound in soy sauce aroma-type Chinese Baijiu J Agric Food Chem 2019 Jul 1767287916 7925 https://doi.org/10.1021/acs.jafc.9b0209510.1021/acs.jafc.9b0209531180675Search in Google Scholar

Zhong Y, Xie YH. [Method for determination of caproic acid content in caproic acid bacteria culture solution] (in Chinese). Liquor Mak Sci Technol. 2004 Apr;04:91–92.Zhong Y Xie YH [Method for determination of caproic acid content in caproic acid bacteria culture solution] (in Chinese) Liquor Mak Sci Technol 2004 Apr0491 92Search in Google Scholar

Zhu X, Tao Y, Liang C, Li X, Wei N, Zhang W, Zhou Y, Yang Y, Bo T. The synthesis of n‑caproate from lactate: a new efficient process for medium-chain carboxylates production. Sci Rep. 2015 Sep 25; 5:14360. https://doi.org/10.1038/srep14360Zhu X Tao Y Liang C Li X Wei N Zhang W Zhou Y Yang Y Bo T The synthesis of n‑caproate from lactate: a new efficient process for medium-chain carboxylates production Sci Rep 2015 Sep 25 514360 https://doi.org/10.1038/srep1436010.1038/srep14360458590826403516Search in Google Scholar

Zischka M, Kuenne C, Blom J, Dabrowski PW, Linke B, Hain T, Nitsche A, Goesmann A, Larsen J, Jensen LB, et al. Complete genome sequence of the porcine isolate Enterococcus faecalis D32. J Bacteriol. 2012 Oct;194(19):5490–5491. https://doi.org/10.1128/JB.01298-12Zischka M Kuenne C Blom J Dabrowski PW Linke B Hain T Nitsche A Goesmann A Larsen J Jensen LB et al Complete genome sequence of the porcine isolate Enterococcus faecalis D32 J Bacteriol 2012 Oct194195490 5491 https://doi.org/10.1128/JB.01298-1210.1128/JB.01298-12345721922965105Search in Google Scholar

Zou W, Zhao C, Luo H. Diversity and function of microbial community in Chinese strong-flavor baijiu ecosystem: A Review. Front Microbiol. 2018 Apr 9;9:671. https://doi.org/10.3389/fmicb.2018.00671Zou W Zhao C Luo H Diversity and function of microbial community in Chinese strong-flavor baijiu ecosystem: A Review Front Microbiol 2018 Apr 99671 https://doi.org/10.3389/fmicb.2018.0067110.3389/fmicb.2018.00671590001029686656Search in Google Scholar