Thermodynamics shapes the biogeography of propionate-oxidizing syntrophs in paddy field soils.
Journal
Environmental microbiology reports
ISSN: 1758-2229
Titre abrégé: Environ Microbiol Rep
Pays: United States
ID NLM: 101499207
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
received:
31
01
2021
accepted:
26
05
2021
pubmed:
6
6
2021
medline:
5
4
2022
entrez:
5
6
2021
Statut:
ppublish
Résumé
Soil biogeochemical processes are not only gauged by the dominant taxa in the microbiome but also depend on the critical functions of its 'rare biosphere' members. Here, we evaluated the biogeographical pattern of 'rare biosphere' propionate-oxidizing syntrophs in 113 paddy soil samples collected across China. The relative abundance, activity and growth potential of propionate-oxidizing syntrophs were analysed to provide a panoramic view of syntroph biogeographical distribution at the continental scale. The relative abundances of four syntroph genera, Syntrophobacter, Pelotomaculum, Smithella and Syntrophomonas were significantly greater at the warm low latitudes than at the cool high latitudes. Correspondingly, propionate degradation was faster in the low latitude soils compared with the high latitude soils. The low rate of propionate degradation in the high latitude soils resulted in a greater increase of the total syntroph relative abundance, probably due to their initial low relative abundances and the longer incubation time for propionate consumption. The mean annual temperature (MAT) is the most important factor shaping the biogeographical pattern of propionate-oxidizing syntrophs, with the next factor being the soil's total sulfur content (TS). We suggest that the effect of MAT is related to the thermodynamic conditions, in which the endergonic constraint of propionate oxidation is leveraged with the increase of MAT. The TS effect is likely due to the ability of some propionate syntrophs to facultatively perform sulfate respiration.
Identifiants
pubmed: 34089233
doi: 10.1111/1758-2229.12981
doi:
Substances chimiques
Propionates
0
Soil
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
684-695Informations de copyright
© 2021 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Bahram, M., Hildebrand, F., Forslund, S.K., Anderson, J.L., Soudzilovskaia, N.A., Bodegom, P.M., et al. (2018) Structure and function of the global topsoil microbiome. Nature 560: 233-237.
Beardmore, R.E., Gudelj, I., Lipson, D.A., and Hurst, L.D. (2011) Metabolic trade-offs and the maintenance of the fittest and the flattest. Nature 472: 342-346.
Boe, K., Batstone, D.J., Steyer, J.-P., and Angelidaki, I. (2010) State indicators for monitoring the anaerobic digestion process. Water Res 44: 5973-5980.
Chen, Y.T., Zeng, Y., Wang, H.Z., Zheng, D., Kamagata, Y., Narihiro, T., et al. (2020) Different interspecies electron transfer patterns during mesophilic and thermophilic syntrophic propionate degradation in chemostats. Microb Ecol 80: 120-132.
Conrad, R. (2009) The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Rep 1: 285-292.
Crowther, T.W., van den Hoogen, J., Wan, J., Mayes, M.A., Keiser, A.D., Mo, L., et al. (2019) The global soil community and its influence on biogeochemistry. Science 365: eaav0550.
de Bok, F.A.M., Stams, A.J.M., Dijkema, C., and Boone, D.R. (2001) Pathway of propionate oxidation by a syntrophic culture of Smithella propionica and Methanospirillum hungatei. Appl Environ Microbiol 67: 1800-1804.
Delgado-Baquerizo, M., Oliverio, A.M., Brewer, T.E., Benavent-Gonzalez, A., Eldridge, D.J., Bardgett, R.D., et al. (2018) A global atlas of the dominant bacteria found in soil. Science 359: 320-325.
Deng, N., Grassini, P., Yang, H., Huang, J., Cassman, K.G., and Peng, S. (2019) Closing yield gaps for rice self-sufficiency in China. Nat Commun 10: 1725.
Dolfing, J. (2013) Syntrophic propionate oxidation via butyrate: a novel window of opportunity under methanogenic conditions. Appl Environ Microbiol 79: 4515-4516.
Dyksma, S., and Gallert, C. (2019) Candidatus Syntrophosphaera thermopropionivorans: a novel player in syntrophic propionate oxidation during anaerobic digestion. Environ Microbiol Rep 11: 558-570.
Gan, Y., Qiu, Q., Liu, P., Rui, J., and 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.
Garbeva, P., van Veen, J.A., and van Elsas, J.D. (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42: 243-270.
Glissmann, K., and Conrad, R. (2000) Fermentation pattern of methanogenic degradation of rice straw in anoxic paddy soil. FEMS Microbiol Ecol 31: 117-126.
Glissmann, K., Weber, S., and Conrad, R. (2001) Localization of processes involved in methanogenic in degradation of rice straw in anoxic paddy soil. Environ Microbiol 3: 502-511.
Guo, X., Feng, J., Shi, Z., Zhou, X., Yuan, M., Tao, X., et al. (2018) Climate warming leads to divergent succession of grassland microbial communities. Nat Clim Change 8: 813-818.
Guo, X., Zhou, X., Hale, L., Yuan, M., Ning, D., Feng, J., et al. (2019) Climate warming accelerates temporal scaling of grassland soil microbial biodiversity. Nat Ecol Evol 3: 612-619.
Haefele, S.M., Nelson, A., and Hijmans, R.J. (2014) Soil quality and constraints in global rice production. Geoderma 235: 250-259.
Hanselmann, K.W. (1991) Microbial energetics applied to waste repositories. Experientia 47: 645-687.
Harmsen, H.J.M., Van Kuijk, B.L.M., Plugge, C.M., Akkermans, A.D.L., De Vos, W.M., and Stams, A.J.M. (1998) Syntrophobacter fumaroxidans sp. nov., a syntrophic propionate-degrading sulfate-reducing bacterium. Int J Syst Bacteriol 48: 1383-1387.
Hidalgo-Ahumada, C.A.P., Nobu, M.K., Narihiro, T., Tamaki, H., Liu, W.-T., Kamagata, Y., et al. (2018) Novel energy conservation strategies and behaviour of Pelotomaculum schinkii driving syntrophic propionate catabolism. Environ Microbiol 20: 4503-4511.
Imachi, H., Sekiguchi, Y., Kamagata, Y., Hanada, S., Ohashi, A., and Harada, H. (2002) Pelotomaculum thermopropionicum gen. nov., sp nov., an anaerobic, thermophilic, syntrophic propionate-oxidizing bacterium. Int J Syst Evol Microbiol 52: 1729-1735.
Imachi, H., Sakai, S., Ohashi, A., Harada, H., Hanada, S., Kamagata, Y., and Sekiguchi, Y. (2007) Pelotomaculum propionicicum sp nov., an anaerobic, mesophilic, obligately syntrophic propionate-oxidizing bacterium. Int J Syst Evol Microbiol 57: 1487-1492.
Imachi, H., Sekiguchi, Y., Kamagata, Y., Loy, A., Qiu, Y.L., Hugenholtz, P., et al. (2006) Non-sulfate-reducing, syntrophic bacteria affiliated with Desulfotomaculum cluster I are widely distributed in methanogenic environments. Appl Environ Microbiol 72: 2080-2091.
Kramer, H., and Conrad, R. (1993) Measurement of dissolved H2 concentrations in methanogenic environments with a gas-siffusion probe. FEMS Microbiol Ecol 12: 149-158.
Krylova, N.I., Janssen, P.H., and Conrad, R. (1997) Turnover of propionate in methanogenic paddy soil. FEMS Microbiol Ecol 23: 107-117.
Li, H.J., Chang, J.L., Liu, P.F., Fu, L., Ding, D.W., and Lu, Y.H. (2015) Direct interspecies electron transfer accelerates syntrophic oxidation of butyrate in paddy soil enrichments. Environ Microbiol 17: 1533-1547.
Li, Y., Sun, Y., Li, L., and Yuan, Z. (2018) Acclimation of acid-tolerant methanogenic propionate-utilizing culture and microbial community dissecting. Bioresour Technol 250: 117-123.
Lipson, D.A. (2015) The complex relationship between microbial growth rate and yield and its implications for ecosystem processes. Front Microbiol 6: 615.
Liu, Y.T., Balkwill, D.L., Aldrich, H.C., Drake, G.R., and Boone, D.R. (1999) Characterization of the anaerobic propioate-degrading syntrophs Smithella propionica gen. nov., sp. nov. and Syntrophobacter wolinii. Int J Syst Bacteriol 49: 545-556.
Lueders, T., Pommerenke, B., and Friedrich, M.W. (2004) Stable-isotope probing of microorganisms thriving at thermodynamic limits: syntrophic propionate oxidation in flooded soil. Appl Environ Microbiol 70: 5778-5786.
Lynch, M.D., and Neufeld, J.D. (2015) Ecology and exploration of the rare biosphere. Nat Rev Microbiol 13: 217-229.
McInerney, M.J., Sieber, J.R., and Gunsalus, R.P. (2009) Syntrophy in anaerobic global carbon cycles. Curr Opin Biotechnol 20: 623-632.
Mueller, N., Worm, P., Schink, B., Stams, A.J.M., and Plugge, C.M. (2010) Syntrophic butyrate and propionate oxidation processes: from genomes to reaction mechanisms. Environ Microbiol Rep 2: 489-499.
Nilsen, R.K., Torsvik, T., and Lien, T. (1996) Desulfotomaculum thermocisternum sp nov, a sulfate reducer isolated from a hot North Sea oil reservoir. Int J Syst Bacteriol 46: 397-402.
Noll, M., Klose, M., and 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.
Peng, J., Wegner, C.-E., Bei, Q., Liu, P., and Liesack, W. (2018) Metatranscriptomics reveals a differential temperature effect on the structural and functional organization of the anaerobic food web in rice field soil. Microbiome 6: 169.
Plugge, C.M., Balk, M., and Stams, A.J.M. (2002) Desulfotomaculum thermobenzoicum subsp thermosyntrophicum subsp nov., a thermophilic, syntrophic, propionate-oxidizing, spore-forming bacterium. Int J Syst Evol Microbiol 52: 391-399.
Qi, W., Liu, S.H., Zhao, M.F., and Liu, Z. (2016) China's different spatial patterns of population growth based on the "Hu Line". J Geogr Sci 26: 1611-1625.
Rebac, S., Visser, A., Gerbens, S., VanLier, J.B., Stams, A.J.M., and Lettinga, G. (1996) The effect of sulphate on propionate and butyrate degradation in a psychrophilic anaerobic expanded granular sludge bed (EGSB) reactor. Environ Technol 17: 997-1005.
Rillig, M.C., Ryo, M., Lehmann, A., Aguilar-Trigueros, C.A., Buchert, S., Wulf, A., et al. (2019) The role of multiple global change factors in driving soil functions and microbial biodiversity. Science 366: 886-890.
Rui, J., Peng, J., and Lu, Y. (2009) Succession of bacterial populations during plant residue decomposition in rice field soil. Appl Environ Microbiol 75: 4879-4886.
Schink, B. (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61: 262-280.
Schink, B., and Stams, A.J.M. (2006) Syntrophism among prokaryotes. In The Prokaryotes. Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.H., and Stackebrandt, E. (eds). New York: Springer, pp. 309-335.
Schlatter, D.C., Bakker, M.G., Bradeen, J.M., and Kinkel, L.L. (2015) Plant community richness and microbial interactions structure bacterial communities in soil. Ecology 96: 134-142.
Schutz, H., Conrad, R., Goodwin, S., and Seiler, W. (1988) Emission of hydrogen from feep and dhallow fresh-water environments. Biogeochemistry 5: 295-311.
Sedano-Nunez, V.T., Boeren, S., Stams, A.J.M., and Plugger, C.M. (2018) Comparative proteome analysis of propionate degradation by Syntrophobacter fumaroxidans in pure culture and in coculture with methanogens. Environ Microbiol 20: 1842-1856.
Seel, W., Derichs, J., and Lipski, A. (2016) Increased biomass production by mesophilic food-associated bacteria through lowering the growth temperature from 30°C to 10°C. Appl Environ Microbiol 82: 3754-3764.
Shock, E.L., and Helgeson, H.C. (1990) Calculation of the thermodynamic and transport-properties of aqueous species at high-pressures and temperatures: standard partial molal properties of organic-species. Geochim Cosmochim Acta 54: 915-945.
Sieber, J.R., McInerney, M.J., and Gunsalus, R.P. (2012) Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation. Annu Rev Microbiol 66: 429-452.
Singh, A., Schnurer, A., and Westerholm, M. (2021) Enrichment and description of novel bacteria performing syntrophic propionate oxidation at high ammonia level. Environ Microbiol 23: 1620-1637. https://doi.org/10.1111/1462-2920.15388.
Stams, A.J., and Plugge, C.M. (2009) Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7: 568-577.
Steidinger, B.S., Crowther, T.W., Liang, J., Van Nuland, M.E., Werner, G.D.A., Reich, P.B., et al. (2019) Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature 569: 404-408.
Thauer, R.K. (1998) Biochemistry of methanogenesis: a tribute to Marjory Stephenson. Microbiology 144: 2377-2406.
Thauer, R.K., Kaster, A.K., Seedorf, H., Buckel, W., and Hedderich, R. (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6: 579-591.
Tveit, A.T., Urich, T., Frenzel, P., and Svenning, M.M. (2015) Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming. Proc Natl Acad Sci USA 112: E2507-E2516.
van den Hoogen, J., Geisen, S., Routh, D., Ferris, H., Traunspurger, W., Wardle, D.A., et al. (2019) Soil nematode abundance and functional group composition at a global scale. Nature 572: 194-198.
Van Kuijk, B.L., and Stams, A.J. (1995) Sulfate reduction by a syntrophic propionate-oxidizing bacterium. Anton Leeuw Int J G 68: 293-296.
Worm, P., Koehorst, J.J., Visser, M., Sedano-Nunez, V.T., Schaap, P.J., Plugge, C.M., et al. (2014) A genomic view on syntrophic versus non-syntrophic lifestyle in anaerobic fatty acid degrading communities. Biochim Biophys Acta 1837: 2004-2016.
Xia, X., Zhang, J., Song, T., and Lu, Y. (2019) Stimulation of Smithella-dominating propionate oxidation in a sediment enrichment by magnetite and carbon nanotubes. Environ Microbiol Rep 11: 236-248.
Zhang, C.Y., Liu, X.L., and Dong, X.Z. (2004) Syntrophomonas curvata sp nov., an anaerobe that degrades fatty acids in co-culture with methanogens. Int J Syst Evol Microbiol 54: 969-973.
Zhou, J., Deng, Y., Shen, L., Wen, C., Yan, Q., Ning, D., et al. (2016) Temperature mediates continental-scale diversity of microbes in forest soils. Nat Commun 7: 12083.