The occurrence and ecology of microbial chain elongation of carboxylates in soils.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
13
07
2020
accepted:
13
01
2021
revised:
14
12
2020
pubmed:
10
2
2021
medline:
6
8
2021
entrez:
9
2
2021
Statut:
ppublish
Résumé
Chain elongation is a growth-dependent anaerobic metabolism that combines acetate and ethanol into butyrate, hexanoate, and octanoate. While the model microorganism for chain elongation, Clostridium kluyveri, was isolated from a saturated soil sample in the 1940s, chain elongation has remained unexplored in soil environments. During soil fermentative events, simple carboxylates and alcohols can transiently accumulate up to low mM concentrations, suggesting in situ possibility of microbial chain elongation. Here, we examined the occurrence and microbial ecology of chain elongation in four soil types in microcosms and enrichments amended with chain elongation substrates. All soils showed evidence of chain elongation activity with several days of incubation at high (100 mM) and environmentally relevant (2.5 mM) concentrations of acetate and ethanol. Three soils showed substantial activity in soil microcosms with high substrate concentrations, converting 58% or more of the added carbon as acetate and ethanol to butyrate, butanol, and hexanoate. Semi-batch enrichment yielded hexanoate and octanoate as the most elongated products and microbial communities predominated by C. kluyveri and other Firmicutes genera not known to undergo chain elongation. Collectively, these results strongly suggest a niche for chain elongation in anaerobic soils that should not be overlooked in soil microbial ecology studies.
Identifiants
pubmed: 33558687
doi: 10.1038/s41396-021-00893-2
pii: 10.1038/s41396-021-00893-2
pmc: PMC8245554
doi:
Substances chimiques
Acetates
0
Soil
0
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1907-1918Références
Barker HA, Taha SM. Clostridium kluyverii, an organism concerned in the formation of caproic acid from ethyl alcohol. J Bacteriol. 1942;43:347–63.
pubmed: 16560506
pmcid: 373609
doi: 10.1128/jb.43.3.347-363.1942
Angenent LT, Richter H, Buckel W, Spirito CM, Steinbusch KJJ, Plugge CM, et al. Chain elongation with reactor microbiomes: open-culture biotechnology to produce biochemicals. Environ Sci Technol. 2016;50:2796–810.
pubmed: 26854969
doi: 10.1021/acs.est.5b04847
Béchamp MA. Lettre de m. A. Béchamp a m. Dumas. Ann Chim Phys 1868;4:103–11.
Weimer PJ, Stevenson DM. Isolation, characterization, and quantification of Clostridium kluyveri from the bovine rumen. Appl Microbiol Biotechnol. 2012;94:461–6.
pubmed: 22159841
doi: 10.1007/s00253-011-3751-z
Kenealy WR, Waselefsky DM. Studies on the substrate range of Clostridium kluyveri - the use of propanol and succinate. Arch Microbiol. 1985;141:187–94.
doi: 10.1007/BF00408056
Barker HA, Kamen MD, Bornstein BT. The synthesis of butyric and caproic acids from ethanol and acetic acid by Clostridium kluyveri. Proc Natl Acad Sci USA. 1945;31:373–81.
pubmed: 16588706
pmcid: 1078850
doi: 10.1073/pnas.31.12.373
Bornstein BT, Barker HA. The energy metabolism of Clostridium kluyveri and the synthesis of fatty acids. J Biol Chem. 1948;172:659–69.
pubmed: 18901185
doi: 10.1016/S0021-9258(19)52752-1
Seedorf H, Fricke WF, Veith B, Bruggemann H, Liesegang H, Strittimatter A, et al. The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features. Proc Natl Acad Sci USA. 2008;105:2128–33.
pubmed: 18218779
pmcid: 2542871
doi: 10.1073/pnas.0711093105
Gonzalez-Cabaleiro R, Lema JM, Rodriguez J, Kleerebezem R. Linking thermodynamics and kinetics to assess pathway reversibility in anaerobic bioprocesses. Energy Environ Sci. 2013;6:3780–9.
doi: 10.1039/c3ee42754d
Spirito CM, Richter H, Rabaey K, Stams AJM, Angenent LT. Chain elongation in anaerobic reactor microbiomes to recover resources from waste. Curr Opin Biotechnol. 2014;27:115–22.
pubmed: 24487179
doi: 10.1016/j.copbio.2014.01.003
Rittmann BE & McCarty PL. Environmental Biotechnology: Principles and Applications. McGraw-Hill Book Education: New York; 2001.
Thauer RK, Jungermann K, Henninger H, Wenning J, Decker K. The energy metabolism of Clostridium kluyveri. Eur J Biochem. 1968;4:173–80.
pubmed: 5655494
doi: 10.1111/j.1432-1033.1968.tb00189.x
Stadtman ER, Barker HA. Fatty acid synthesis by enzyme preparations of Clostridium kluyveri. I. Preparation of cell-free extracts that catalyze the conversion of ethanol and acetate to butyrate and caproate. J Biol Chem. 1949;180:1085–93.
pubmed: 18139204
doi: 10.1016/S0021-9258(19)51223-6
Stadtman ER, Barker HA. Fatty acid synthesis by enzyme preparations of Clostridium kluyveri. VI. Reactions of acyl phosphates. J Biol Chem. 1950;184:769–93.
pubmed: 15428461
doi: 10.1016/S0021-9258(19)51011-0
Steinbusch KJJ, Hamelers HVM, Plugge CM, Buisman CJN. Biological formation of caproate and caprylate from acetate: fuel and chemical production from low grade biomass. Energy Environ Sci. 2011;4:216–24.
doi: 10.1039/C0EE00282H
Agler MT, Spirito CM, Usack JG, Werner JJ, Angenent LT. Chain elongation with reactor microbiomes: upgrading dilute ethanol to medium-chain carboxylates. Energy Environ Sci. 2012;5:8189–92.
doi: 10.1039/c2ee22101b
Cavalcante WD, Leitao RC, Gehring TA, Angenent LT, Santaella ST. Anaerobic fermentation for n-caproic acid production: A review. Process Biochem. 2017;54:106–19.
doi: 10.1016/j.procbio.2016.12.024
De Groof V, Coma M, Arnot T, Leak DJ, Lanham AB. Medium chain carboxylic acids from complex organic feedstocks by mixed culture fermentation. Molecules 2019;24:398.
pmcid: 6384945
doi: 10.3390/molecules24030398
Schievano A, Sciarria TP, Vanbroekhoven K, De Wever H, Puig S, Andersen SJ, et al. Electro-fermentation - merging electrochemistry with fermentation in industrial applications. Trends Biotechnol. 2016;34:866–78.
pubmed: 27173172
doi: 10.1016/j.tibtech.2016.04.007
Jourdin L, Raes SMT, Buisman CJN, Strik D. Critical biofilm growth throughout unmodified carbon felts allows continuous bioelectrochemical chain elongation from CO
doi: 10.3389/fenrg.2018.00007
Candry P, Huang SL, Carvajal-Arroyo JM, Rabaey K, Ganigue R. Enrichment and characterisation of ethanol chain elongating communities from natural and engineered environments. Sci Rep. 2020;10:1–10.
doi: 10.1038/s41598-020-60052-z
Conrad R. Importance of hydrogenotrophic, aceticlastic and methylotrophic methanogenesis for methane production in terrestrial, aquatic and other anoxic environments: a mini review. Pedosphere 2020;30:25–39.
doi: 10.1016/S1002-0160(18)60052-9
Rui JP, Peng JJ, Lu YH. Succession of bacterial populations during plant residue decomposition in rice field soil. Appl Environ Microbiol. 2009;75:4879–86.
pubmed: 19465536
pmcid: 2708425
doi: 10.1128/AEM.00702-09
Tsutsuki K, Ponnamperuma FN. Behavior of anaerobic decomposition in submerged soils - effect of organic material amendment, soil properties, and temperature. Soil Sci Plant Nutr. 1987;33:13–33.
doi: 10.1080/00380768.1987.10557549
Roy R, Kluber HD, Conrad R. Early initiation of methane production in anoxic rice soil despite the presence of oxidants. FEMS Microbiol Ecol. 1997;24:311–20.
doi: 10.1111/j.1574-6941.1997.tb00448.x
Adeleke R, Nwangburuka C, Oboirien B. Origins, roles and fate of organic acids in soils: a review. S Afr J Bot. 2017;108:393–406.
doi: 10.1016/j.sajb.2016.09.002
Mohana Rangan S, Mouti A, LaPat-Polasko L, Lowry GV, Krajmalnik-Brown R, Delgado A. Synergistic zero-valent iron (Fe
doi: 10.1021/acs.est.0c05052
Delgado AG, Kang D-W, Nelson KG, Fajardo-Williams D, Miceli JF, III, Done HY, et al. Selective enrichment yields robust ethene-producing dechlorinating cultures from microcosms stalled at cis-dichloroethene. PLoS ONE. 2014;9:e100654.
pubmed: 24950250
pmcid: 4065118
doi: 10.1371/journal.pone.0100654
Delgado AG, Fajardo-Williams D, Popat SC, Torres CI, Krajmalnik-Brown R. Successful operation of continuous reactors at short retention times results in high-density, fast-rate Dehalococcoides dechlorinating cultures. Appl Microbiol Biotechnol. 2014;98:2729–37.
pubmed: 24085396
doi: 10.1007/s00253-013-5263-5
Chen TF, Delgado AG, Yavuz BM, Maldonado J, Zuo Y, Kamath R, et al. Interpreting interactions between ozone and residual petroleum hydrocarbons in soil. Environ Sci Technol. 2017;51:506–13.
pubmed: 27973790
doi: 10.1021/acs.est.6b04534
Esquivel-Elizondo S, Miceli J, Torres CI, Krajmalnik-Brown R. Impact of carbon monoxide partial pressures on methanogenesis and medium chain fatty acids production during ethanol fermentation. Biotechnol Bioeng. 2018;115:341–50.
pubmed: 28987001
doi: 10.1002/bit.26471
Delgado AG, Fajardo-Williams D, Kegerreis KL, Parameswaran P, Krajmalnik-Brown R. Impact of ammonium on syntrophic organohalide-respiring and fermenting microbial communities. mSphere. 2016;1:e00053–16.
pubmed: 27303735
pmcid: 4894693
doi: 10.1128/mSphere.00053-16
Delgado AG, Fajardo-Williams D, Bondank E, Esquivel-Elizondo S, Krajmalnik-Brown R. Coupling bioflocculation of Dehalococcoides mccartyi to high-rate reductive dehalogenation of chlorinated ethenes. Environ Sci Technol. 2017;51:11297–307.
pubmed: 28914537
doi: 10.1021/acs.est.7b03097
Esquivel-Elizondo S, Delgado AG, Krajmalnik-Brown R. Evolution of microbial communities growing with carbon monoxide, hydrogen, and carbon dioxide. FEMS Microbiol Ecol. 2017;93:fix076.
doi: 10.1093/femsec/fix076
Xiaoyu Z, Yong T, Cheng L, Xiangzhen L, Na W, Wenjie Z, et al. The synthesis of n-caproate from lactate: a new efficient process for medium-chain carboxylates production. Sci Rep. 2015;5:14360.
doi: 10.1038/srep14360
Caporaso JG, Christian LL, William AW, Donna B-L, James H, Noah F, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621–24.
pubmed: 22402401
pmcid: 3400413
doi: 10.1038/ismej.2012.8
Masella A, Bartram A, Truszkowski J, Brown D, Neufeld J. PANDAseq: paired-end assembler for illumina sequences. BMC Bioinform. 2012;13:31.
doi: 10.1186/1471-2105-13-31
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–57.
pubmed: 31341288
pmcid: 7015180
doi: 10.1038/s41587-019-0209-9
Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 2017;11:2639–43.
pubmed: 28731476
pmcid: 5702726
doi: 10.1038/ismej.2017.119
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–D6.
pubmed: 23193283
doi: 10.1093/nar/gks1219
Robeson MS, O’Rourke DR, Kaehler BD, Ziemski M, Dillon MR, Foster JT, et al. RESCRIPt: Reproducible sequence taxonomy reference database management for the masses. bioRxiv. 2020; https://doi.org/10.1101/2020.10.05.326504 .
Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, et al. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome. 2018;6:90.
pubmed: 29773078
pmcid: 5956843
doi: 10.1186/s40168-018-0470-z
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST plus: architecture and applications. BMC Bioinform. 2009;10:1.
doi: 10.1186/1471-2105-10-421
Kusel K, Drake HL. Acetate synthesis in soil from a Bavarian beech forest. Appl Environ Microbiol. 1994;60:1370–3.
pubmed: 16349243
pmcid: 201485
doi: 10.1128/aem.60.4.1370-1373.1994
Kusel K, Drake HL. Effects of environmental parameters on the formation and turnover of acetate by forest soils. Appl Environ Microbiol. 1995;61:3667–75.
pubmed: 16535147
pmcid: 1388709
doi: 10.1128/aem.61.10.3667-3675.1995
Duddleston KN, Kinney MA, Kiene RP, Hines ME. Anaerobic microbial biogeochemistry in a northern bog: Acetate as a dominant metabolic end product. Glob Biogeochem Cycles. 2002;16:11.1–9.
doi: 10.1029/2001GB001402
Thebrath B, Mayer HP, Conrad R. Bicarbonate-dependent production and methanogenic consumption of acetate in anoxic paddy soil. FEMS Microbiol Ecol. 1992;86:295–302.
doi: 10.1111/j.1574-6968.1992.tb04821.x
Delgado AG, Parameswaran P, Fajardo-Williams D, Halden RU, Krajmalnik-Brown R. Role of bicarbonate as a pH buffer and electron sink in microbial dechlorination of chloroethenes. Microb Cell Fact. 2012;11:128.
pubmed: 22974059
pmcid: 3511292
doi: 10.1186/1475-2859-11-128
Kucek LA, Spirito CM, Angenent LT. High n-caprylate productivities and specificities from dilute ethanol and acetate: chain elongation with microbiomes to upgrade products from syngas fermentation. Energy Environ Sci. 2016;9:3482–94.
doi: 10.1039/C6EE01487A
Volker AR, Gogerty DS, Bartholomay C, Hennen-Bierwagen T, Zhu HL, Bobik TA. Fermentative production of short-chain fatty acids in Escherichia coli. Microbiology 2014;160:1513–22.
pubmed: 24722906
doi: 10.1099/mic.0.078329-0
Grootscholten TIM, Steinbusch KJJ, Hamelers HVM, Buisman CJN. Chain elongation of acetate and ethanol in an upflow anaerobic filter for high rate MCFA production. Bioresour Technol. 2013;135:440–5.
pubmed: 23228455
doi: 10.1016/j.biortech.2012.10.165
Reddy MV, Mohan SV, Chang YC. Medium-chain fatty acids (MCFA) production through anaerobic fermentation using Clostridium kluyveri: effect of ethanol and acetate. Appl Biochem Biotechnol. 2018;185:594–605.
pubmed: 29247333
doi: 10.1007/s12010-017-2674-2
Scarborough MJ, Lawson CE, Hamilton JJ, Donohue TJ, Noguera DR. Metatranscriptomic and thermodynamic insights into medium-chain fatty acid production using an anaerobic microbiome. mSystems 2018;3:6.
doi: 10.1128/mSystems.00221-18
Bao S, Wang QY, Zhang PY, Zhang Q, Wu Y, Li F, et al. Effect of acid/ethanol ratio on medium chain carboxylate production with different VFAs as the electron acceptor: insight into carbon balance and microbial community. Energies 2019;12:3720.
doi: 10.3390/en12193720
Spirito CM, Marzilli AM, Angenent LT. Higher substrate ratios of ethanol to acetate steered chain elongation toward n-caprylate in a bioreactor with product extraction. Environ Sci Technol. 2018;52:13438–47.
pubmed: 30335369
doi: 10.1021/acs.est.8b03856
Coma M, Vilchez-Vargas R, Roume H, Jauregui R, Pieper DH, Rabaey K. Product diversity linked to substrate usage in chain elongation by mixed-culture fermentation. Environ Sci Technol. 2016;50:6467–76.
pubmed: 27162101
doi: 10.1021/acs.est.5b06021
Janssen PH. Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol. 2006;72:1719–28.
pubmed: 16517615
pmcid: 1393246
doi: 10.1128/AEM.72.3.1719-1728.2006
Spain AM, Krumholz LR, Elshahed MS. Abundance, composition, diversity and novelty of soil Proteobacteria. ISME J 2009;3:992–1000.
pubmed: 19404326
doi: 10.1038/ismej.2009.43
Johnson JS, Spakowicz DJ, Hong BY, Petersen LM, Demkowicz P, Chen L, et al. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat Commun. 2019;10:5029.
pubmed: 31695033
pmcid: 6834636
doi: 10.1038/s41467-019-13036-1
Hollister EB, Forrest AK, Wilkinson HH, Ebbole DJ, Malfatti SA, Tringe SG, et al. Structure and dynamics of the microbial communities underlying the carboxylate platform for biofuel production. Appl Microbiol Biotechnol. 2010;88:389–99.
pubmed: 20676626
doi: 10.1007/s00253-010-2789-7
Mackie RI, Aminov RI, Hu WP, Klieve AV, Ouwerkerk D, Sundset MA, et al. Ecology of uncultivated Oscillospira species in the rumen of cattle, sheep, and reindeer as assessed by microscopy and molecular approaches. Appl Environ Microbiol. 2003;69:6808–15.
pubmed: 14602644
pmcid: 262257
doi: 10.1128/AEM.69.11.6808-6815.2003
Ye TR, Cai HY, Liu X, Jiang HL. Dominance of Oscillospira and Bacteroides in the bacterial community associated with the degradation of high-concentration dimethyl sulfide under iron-reducing condition. Ann Microbiol. 2016;66:1199–206.
doi: 10.1007/s13213-016-1207-5
Konikoff T, Gophna U. Oscillospira: a central, enigmatic component of the human gut microbiota. Trends Microbiol. 2016;24:523–4.
pubmed: 26996766
doi: 10.1016/j.tim.2016.02.015
Clarke RTJ. Niche in pasture-fed ruminants for the large rumen bacteria Oscillospira, Lampropedia, and Quin’s and Eadie’s ovals. Appl Environ Microbiol. 1979;37:654–7.
pubmed: 16345363
pmcid: 243270
doi: 10.1128/aem.37.3.654-657.1979
Lee GH, Rhee MS, Chang DH, Lee J, Kim S, Yoon MH, et al. Oscillibacter ruminantium sp nov., isolated from the rumen of Korean native cattle. Int J Syst Evol Microbiol. 2013;63:1942–6.
pubmed: 23024142
doi: 10.1099/ijs.0.041749-0
Iino T, Mori K, Tanaka K, Suzuki KI, Harayama S. Oscillibacter valericigenes gen. nov., sp nov., a valerate-producing anaerobic bacterium isolated from the alimentary canal of a Japanese corbicula clam. Int J Syst Evol Microbiol. 2007;57:1840–5.
pubmed: 17684268
doi: 10.1099/ijs.0.64717-0
Gophna U, Konikoff T, Nielsen HB. Oscillospira and related bacteria - From metagenomic species to metabolic features. Environ Microbiol. 2017;19:835–41.
pubmed: 28028921
doi: 10.1111/1462-2920.13658
Wang H-J, Dai K, Wang Y-Q, Wang H-F, Zhang F, Zeng RJ. Mixed culture fermentation of synthesis gas in the microfiltration and ultrafiltration hollow-fiber membrane biofilm reactors. Bioresour Technol. 2018;267:650–6.
pubmed: 30059945
doi: 10.1016/j.biortech.2018.07.098
Fraj B, Ben Hania W, Postec A, Hamdi M, Ollivier B, Fardeau ML. Fonticella tunisiensis gen. nov., sp nov., isolated from a hot spring. Int J Syst Evol Microbiol. 2013;63:1947–50.
pubmed: 23024143
doi: 10.1099/ijs.0.041947-0
Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandezgarayzabal J, Garcia P, et al. The phylogeny of the genus Clostridium - Proposal of 5 new genera and 11 new species combinations. Int J Syst Bacteriol. 1994;44:812–26.
pubmed: 7981107
doi: 10.1099/00207713-44-4-812
BS Jeon, Kim BC, Um Y, et al. BI. Production of hexanoic acid from D-galactitol by a newly isolated Clostridium sp. BS-1. Appl Microbiol Biotechnol. 2010;88:1161–7.
doi: 10.1007/s00253-010-2827-5
Zhu XY, Zhou Y, Wang Y, Wu TT, Li XZ, Li DP, et al. Production of high-concentration n-caproic acid from lactate through fermentation using a newly isolated Ruminococcaceae bacterium CPB6. Biotechnol Biofuels. 2017;10:102.
pubmed: 28439295
pmcid: 5399333
doi: 10.1186/s13068-017-0788-y
Robertson WJ, Bowman JP, Franzmann PD, Mee BJ. Desulfosporosinus meridiei sp nov., a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwater. Int J Syst Evol Microbiol. 2001;51:133–40.
pubmed: 11211250
doi: 10.1099/00207713-51-1-133
Lee YJ, Romanek CS, Wiegel J. Desulfosporosinus youngiae sp nov., a spore-forming, sulfate-reducing bacterium isolated from a constructed wetland treating acid mine drainage. Int J Syst Evol Microbiol. 2009;59:2743–6.
pubmed: 19625426
doi: 10.1099/ijs.0.007336-0