Abstract
Propionate is one of the major intermediates in anaerobic digestion of organic waste to CO2 and CH4. In methanogenic environments, propionate is degraded through a mutualistic interaction between symbiotic propionate oxidizers and methanogens. Although temperature heavily influences the microbial ecology and performance of methanogenic processes, its effect on syntrophic interaction during propionate degradation remains poorly understood. In this study, metagenomics and metatranscriptomics were employed to compare mesophilic and thermophilic propionate degradation communities. Mesophilic propionate degradation involved multiple syntrophic organisms (Syntrophobacter, Smithella, and Syntrophomonas), pathways, interactions, and preference toward formate-based electron transfer to methanogenic partners (i.e., Methanoculleus). In thermophilic propionate degradation, one syntrophic organism predominated (Pelotomaculum), interspecies H2 transfer played a major role, and phylogenetically and metabolically diverse H2-oxidizing methanogens were present (i.e., Methanoculleus, Methanothermobacter, and Methanomassiliicoccus). This study showed that microbial interactions, metabolic pathways, and niche diversity are distinct between mesophilic and thermophilic microbial communities responsible for syntrophic propionate degradation.
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References
Koch M, Dolfing J, Wuhrmann K, Zehnder AJB (1983) Pathways of propionate degradation by enriched methanogenic cultures. Appl Environ Microbiol 45:1411–1414. https://doi.org/10.1016/0005-2728(84)90100-2
Schink B, Stams AJM (2002) Syntrophism among prokaryotes. In: Dworkin M (ed) The prokaryotes: an evolving electronic resource for the microbiological community3rd edn. Springer, Berlin
de Bok FA, Stams AJ, Dijkema C, Boone DR (2001) Pathway of propionate oxidation by a syntrophic culture of Smithella propionica and Methanospirillum hungatei. Appl Environ Microbiol 67:1800–1804. https://doi.org/10.1128/AEM.67.4.1800-1804.2001
de Bok FA, Plugge CM, Stams AJ (2004) Interspecies electron transfer in methanogenic propionate degrading consortia. Water Res 38:1368–1375. https://doi.org/10.1016/j.watres.2003.11.028
de Bok FA, Harmsen HJ, Plugge CM, de Vries MC, Akkermans AD, de Vos WM et al (2005) The first true obligately syntrophic propionate-oxidizing bacterium, Pelotomaculum schinkii sp. nov., co-cultured with Methanospirillum hungatei, and emended description of the genus Pelotomaculum. Int J Syst Evol Microbiol 55:1697–1703. https://doi.org/10.1099/ijs.0.02880-0
Hidalgo-Ahumada CA, Nobu MK, Narihiro T, Tamaki H, Liu WT, Kamagata Y et al (2018) Novel energy conservation strategies and behaviour of Pelotomaculum schinkii driving syntrophic propionate catabolism. Environ Microbiol 20:4503–4511. https://doi.org/10.1111/1462-2920.14388
Embree M, Liu JK, Al-Bassam MM, Zengler K (2015) Networks of energetic and metabolic interactions define dynamics in microbial communities. Proc Natl Acad Sci U S A 112:15450–15455. https://doi.org/10.1073/pnas.1506034112
Harmsen HJ, Wullings B, Akkermans AD, Ludwig W, Stams AJ (1993) Phylogenetic analysis of Syntrophobacter wolinii reveals a relationship with sulfate-reducing bacteria. Arch Microbiol 160:238–240. https://doi.org/10.1007/BF00249130
Wallrabenstein C, Hauschild E, Schink B (1995) Syntrophobacter pfennigii sp. nov., new syntrophically propionate-oxidizing anaerobe growing in pure culture with propionate and sulfate. Arch Microbiol 164:346–352. https://doi.org/10.1007/s002030050273
Harmsen HJM, Van Kuijk BLM, Plugge CM, Akkermans ADL, De Vos WM, Stams AJM (1998) Syntrophobacter fumaroxidans sp. nov., a syntrophic propionate-degrading sulfate-reducing bacterium. Int J Syst Bacteriol 48:1383–1387. https://doi.org/10.1099/00207713-48-4-1383
Stams AJ, Plugge CM (2009) Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7:568–577. https://doi.org/10.1038/nrmicro2166
Liu Y, Balkwill DL, Aldrich HC, Drake GR, Boone DR (1999) Characterization of the anaerobic propionate-degrading syntrophs Smithella propionica gen. Nov., sp. nov. and Syntrophobacter wolinii. Int J Syst Bacteriol 49:545–556. https://doi.org/10.1099/00207713-49-2-545
Sieber JR, Mcinerney MJ, Gunsalus RP (2012) Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation. Annu Rev Microbiol 66:429–452. https://doi.org/10.1146/annurev-micro-090110-102844
Narihiro T (2016) Microbes in the water infrastructure: underpinning our society. Microbes Environ 31:89–92. https://doi.org/10.1264/jsme2.ME3102rh
Shen L, Zhao Q, Wu X, Li X, Li Q, Wang Y (2016) Interspecies electron transfer in syntrophic methanogenic consortia: from cultures to bioreactors. Renew Sust Energ Rev 54:1358–1367. https://doi.org/10.1016/j.rser.2015.10.102
Rotaru AE, Shrestha PM, Liu F, Markovaite B, Chen S, Nevin KP et al (2014) Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl Environ Microbiol 80:4599–4605. https://doi.org/10.1128/AEM.00895-14
Kosaka T, Kato S, Shimoyama T, Ishii S, Abe T, Watanabe K (2008) The genome of Pelotomaculum thermopropionicum reveals niche-associated evolution in anaerobic microbiota. Genome Res 18:442–448. https://doi.org/10.1101/gr.7136508
Sieber JR, Sims DR, Han C, Kim E, Lykidis A, Lapidus AL et al (2010) The genome of Syntrophomonas wolfei: new insights into syntrophic metabolism and biohydrogen production. Environ Microbiol 12:2289–2301. https://doi.org/10.1111/j.1462-2920.2010.02237.x
Plugge CM, Henstra AM, Worm P, Swarts DC, Paulitsch-Fuchs AH, Scholten JC et al (2012) Complete genome sequence of Syntrophobacter fumaroxidans strain (MPOBT). Stand Genomic Sci 7:91–106. https://doi.org/10.4056/sigs.2996379
Nobu MK, Narihiro T, Rinke C, Kamagata Y, Tringe SG, Woyke T et al (2015a) Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor. ISME J 9:1710–1722. https://doi.org/10.1038/ismej.2014.256
Nobu MK, Narihiro T, Hideyuki T, Qiu YL, Sekiguchi Y, Woyke T et al (2015b) The genome of Syntrophorhabdus aromaticivorans strain UI provides new insights for syntrophic aromatic compound metabolism and electron flow. Environ Microbiol 17:4861–4872. https://doi.org/10.1111/1462-2920.12444
Nobu MK, Narihiro T, Kuroda K, Mei R, Liu WT (2016) Chasing the elusive Euryarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen. ISME J 10:2478–2487. https://doi.org/10.1038/ismej.2016.33
Ishii S, Kosaka T, Hori K, Hotta Y, Watanabe K (2005) Coaggregation facilitates interspecies hydrogen transfer between Pelotomaculum thermopropionicum and Methanothermobacter thermautotrophicus. Appl Environ Microbiol 71:7838–7845. https://doi.org/10.1128/AEM.71.12.7838-7845.2005
Westermann P, Ahring BK, Mah RA (1989) Temperature compensation in Methanosarcina barkeri by modulation of hydrogen and acetate affinity. Appl Environ Microbiol 55:1262–1266. https://doi.org/10.1016/0167-7799(89)90027-9
Thauer R, Kaster A, Seedorf HW, Hedderich R (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6:579–591. https://doi.org/10.1038/nrmicro1931
Yvon-Durocher G, Allen AP, Bastviken D, Conrad R, Gudasz C, St-Pierre A et al (2014) Methane fluxes show consistent temperature dependence across microbial to ecosystem scales. Nature 507:488–491. https://doi.org/10.1038/nature13164
Tang YQ, Matsui T, Morimura S, Wu XL, Kida K (2008) Effect of temperature on microbial community of a glucose-degrading methanogenic consortium under hyperthermophilic chemostat cultivation. J Biosci Bioeng 106:180–187. https://doi.org/10.1263/jbb.106.180
Gan Y, Qiu Q, Liu P, Rui J, Lu Y (2012) Syntrophic oxidation of propionate in rice field soil at 15 and 30 °C under methanogenic conditions. Appl Environ Microbiol 78:4923–4932. https://doi.org/10.1128/AEM.00688-12
Conrad R, Klose M, Noll M (2009) Functional and structural response of the methanogenic microbial community in rice field soil to temperature change. Environ Microbiol 11:1844–1853. https://doi.org/10.1111/j.1462-2920.2009.01909.x
Boone DR, Johnson RL, Liu Y (1989) Diffusion of the interspecies electron carriers H2 and formate in methanogenic ecosystems and its implications in the measurement of Km for H2 or formate uptake. Appl Environ Microbiol 55:1735–1741. https://doi.org/10.1088/0032-1028/16/10/002
Fey A, Chin KJ, Conrad R (2001) Thermophilic methanogens in rice field soil. Environ Microbiol 3:295–303. https://doi.org/10.1046/j.1462-2920.2001.00195.x
Fey A, Claus P, Conrad R (2004) Temporal change of 13C isotope signatures and methanogenic pathways in rice field soil incubated anoxically at different temperatures. Geochim Cosmochim Acta 68:293–306. https://doi.org/10.1016/S0016-7037(03)00426-5
Noll M, Klose M, Conrad R (2010) Effect of temperature change on the composition of the bacterial and archaeal community potentially involved in the turnover of acetate and propionate in methanogenic rice field soil. FEMS Microbiol Ecol 73:215–225. https://doi.org/10.1111/j.1574-6941.2010.00883.x
Hua ZS, Han YJ, Chen LX, Liu J, Hu M, Li SJ et al (2015) Ecological roles of dominant and rare prokaryotes in acid mine drainage revealed by metagenomics and metatranscriptomics. ISME J 9:1280–1294. https://doi.org/10.1038/ismej.2014.212
Nobu MK, Narihiro T, Liu M, Kuroda K, Mei R, Liu WT (2017) Thermodynamically diverse syntrophic aromatic compound catabolism. Environ Microbiol 19:4576–4586. https://doi.org/10.1111/1462-2920.13922
Shigematsu T, Tang Y, Kawaguchi H, Ninomiya K, Kijima J, Kobayashi T, Morimura S, Kida K (2003) Effect of dilution rate on structure of a mesophilic acetate-degrading methanogenic community during continuous cultivation. J Biosci Bioeng 96:547–558. https://doi.org/10.1016/s1389-1723(04)70148-6
Griffiths RI, Whiteley AS, O'Donnell AG, Bailey MJ (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488–5491. https://doi.org/10.1128/AEM.66.12.5488-5491.2000
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Wu YW, Simmons BA, Singer SW (2016) MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics 32:605–607. https://doi.org/10.1093/bioinformatics/btv638
Wu YW, Tang YH, Tringe SG, Simmons BA, Singer SW (2014) MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm. Microbiome 2:26. https://doi.org/10.1186/2049-2618-2-26
Kang DD, Froula J, Egan R, Wang Z (2015) MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. Peerj 3:e1165. https://doi.org/10.7717/peerj.1165
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055. https://doi.org/10.1101/gr.186072.114
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. https://doi.org/10.1093/bioinformatics/btu153
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1093/10.1038/nmeth.1923
Langmead B, Wilks C, Antonescu V, Charles R (2018) Scaling read aligners to hundreds of threads on general-purpose processors. Bioinformatics 35:421–432. https://doi.org/10.1093/bioinformatics/bty648
Labatut RA, Angenent LT, Scott NR (2014) Conventional mesophilic vs. thermophilic anaerobic digestion: a trade-off between performance and stability? Water Res 53:249–258. https://doi.org/10.1016/j.watres.2014.01.035
Speece RE, Boonyakitsombut S, Kim M, Azbar N, Ursillo P (2006) Overview of anaerobic treatment: thermophilic and propionate implications. Water Environ Res 78:460–473. https://doi.org/10.2175/106143006X95492
Wilson CA, Murthy SM, Fang Y, Novak JT (2008) The effect of temperature on the performance and stability of thermophilic anaerobic digestion. Water Sci Technol 57:297–304. https://doi.org/10.2166/wst.2008.027
Schmidt JE, Ahring BK (1993) Effects of hydrogen and formate on the degradation of propionate and butyrate in thermophilic granules from an upflow anaerobic sludge blanket reactor. Appl Environ Microbiol 59:2546–2551. https://doi.org/10.1002/bit.260420422
Miller CS, Baker BJ, Thomas BC, Singer SW, Banfield JF (2011) EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Genome Biol 12:R44. https://doi.org/10.1186/gb-2011-12-5-r44
Imachi H, Sekiguchi Y, Kamagata Y, Hanada S, Ohashi A, Harada H (2002) Pelotomaculum thermopropionicum gen. Nov., sp nov., an anaerobic, thermophilic, syntrophic propionate-oxidizing bacterium. Int J Syst Evol Microbiol 52:1729–1735. https://doi.org/10.1099/ijs.0.02212-0
Suryawanshi PC, Chaudhari AB, Kothari RM (2010) Thermophilic anaerobic digestion: the best option for waste treatment. Crit Rev Biotechnol 30:31–40. https://doi.org/10.3109/07388550903330505
Schnürer A, Zellner G, Svensson BH (1999) Mesophilic syntrophic acetate oxidation during methane formation in biogas reactors. FEMS Microbiol Ecol 29:249–261. https://doi.org/10.1016/S0168-6496(99)00016-1
Dolfing J, Larter SR, Head IM (2008) Thermodynamic constraints on methanogenic crude oil biodegradation. ISME J 2:442–452. https://doi.org/10.1038/ismej.2007.111
Dridi B, Fardeau ML, Ollivier B, Raoult D, Drancourt M (2012) Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Microbiol 62:1902–1907. https://doi.org/10.1099/ijs.0.033712-0
Buckel W, Thauer RK (2013) Energy conservation via electron bifurcating ferredoxin reduction and proton/Na(+) translocating ferredoxin oxidation. Biochim Biophys Acta 1827:94–113. https://doi.org/10.1016/j.bbabio.2012.07.002
Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501. https://doi.org/10.1111/j.1574-6976.2001.tb00587.x
Biegel E, Schmidt S, González JM, Müller V (2011) Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes. Cell Mol Life Sci 68:613–634. https://doi.org/10.1007/s00018-010-0555-8
Lang K, Schuldes J, Klingl A, Poehlein A, Daniel R, Brune A (2015) New mode of energy metabolism in the seventh order of methanogens as revealed by comparative genome analysis of “Candidatus Methanoplasma termitum”. Appl Environ Microbiol 81:1338–1352. https://doi.org/10.1128/AEM.03389-14
Welte C, Deppenmeier U (2014) Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens. Biochim Biophys Acta 1837:1130–1147. https://doi.org/10.1016/j.bbabio.2013.12.002
Gargi K, Kridelbaugh DM, Guss AM, Metcalf WW (2009) Hydrogen is a preferred intermediate in the energy-conserving electron transport chain of Methanosarcina barkeri. Proc Natl Acad Sci U S A 106:15915–15920. https://doi.org/10.1073/pnas.0905914106
Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180
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This work was financially supported by the Ministry of Science and Technology of China (2016YFE0127700), the National Natural Science Foundation of China (51678378 and 41701295), the China Postdoctoral Science Foundation (2018 M643480), and the Fundamental Research Funds for the Central University (2018SCUH0023).
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Chen, YT., Zeng, Y., Wang, HZ. et al. Different Interspecies Electron Transfer Patterns during Mesophilic and Thermophilic Syntrophic Propionate Degradation in Chemostats. Microb Ecol 80, 120–132 (2020). https://doi.org/10.1007/s00248-020-01485-x
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DOI: https://doi.org/10.1007/s00248-020-01485-x