nir gene-based co-occurrence patterns reveal assembly mechanisms of soil denitrifiers in response to fire
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
SEJI/2017/030
Generalitat Valenciana
CGL2017-89751-R
Ministerio de Economía y Competitividad
PubMed
33118311
DOI
10.1111/1462-2920.15298
Knihovny.cz E-zdroje
- MeSH
- Bacteria genetika metabolismus MeSH
- denitrifikace genetika fyziologie MeSH
- dusičnany metabolismus MeSH
- dusík metabolismus MeSH
- ekosystém MeSH
- nitritreduktasy genetika metabolismus MeSH
- požáry * MeSH
- půda chemie MeSH
- půdní mikrobiologie MeSH
- salinita MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- dusičnany MeSH
- dusík MeSH
- nitritreduktasy MeSH
- půda MeSH
Denitrification causes nitrogen losses from terrestrial ecosystems. The magnitude of nitrogen loss depends on the prevalence of denitrifiers, which show ecological differences if they harbour nirS or nirK genes encoding nitrite reductases with the same biological function. Thus, it is relevant to understand the mechanisms of co-existence of denitrifiers, including their response to environmental filters and competition due to niche similarities. We propose a framework to analyse the co-existence of denitrifiers across multiple assemblages by using nir gene-based co-occurrence networks. We applied it in Mediterranean soils before and during 1 year after an experimental fire. Burning did not modify nir community structure, but significantly impacted co-occurrence patterns. Bacteria with the same nir co-occurred in space, and those with different nir excluded each other, reflecting niche requirements: nirS abundance responded to nitrate and salinity, whereas nirK to iron content. Prior to fire, mutual exclusion between bacteria with the same nir suggested competition due to niche similarities. Burning provoked an immediate rise in mineral nitrogen and erased the signals of competition, which emerged again within days as nir abundances peaked. nir co-occurrence patterns can help infer the assembly mechanisms of denitrifying communities, which control nitrogen losses in the face of ecological disturbance.
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Andersson, M., Michelsen, A., Jensen, M., and Kjøller, A. (2004) Tropical savannah woodland: effects of experimental fire on soil microorganisms and soil emissions of carbon dioxide. Soil Biol Biochem 36: 849-858.
Barberán, A., Bates, S.T., Casamayor, E.O., and Fierer, N. (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6: 343-351.
Baselga, A. (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19: 134-143.
Baselga, A., Orme, D., Villeger, S., De Bortoli, J., and Leprieur, F. (2018) Betapart: partitioning beta diversity into turnover and nestedness components. R package v 1.5.0 https://cran.r-project.org/web/packages/betapart/index.html
Bonilla-Rosso, G., Wittorf, L., Jones, C.M., and Hallin, S. (2016) Design and evaluation of primers targeting genes encoding NO-forming nitrite reductases: implications for ecological inference of denitrifying communities. Sci Rep 6: 39208. https://doi.org/10.1038/srep39208.
Braker, G., Fesefeldt, A., and Witzel, K.P. (1998) Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microbiol 64: 3769-3775.
Bru, D., Ramette, A., Saby, N.P.A., Dequiedt, S., Ranjard, L., Jolivet, C., et al. (2011) Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. ISME J 5: 532-542.
Canfield, D.E., Glazer, A.N., and Falkowski, P.G. (2010) The evolution and future of Earth's nitrogen cycle. Science 330: 192-196.
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Meth 7: 335-336.
Castaldi, S., and Aragosa, D. (2002) Factors influencing nitrification and denitrification variability in a natural and fire-disturbed Mediterranean shrubland. Biol Fertil Soils 36: 418-425.
Certini, G. (2005) Effects of fire on properties of forest soils: a review. Oecologia 143: 1-10.
Chesson, P. (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31: 343-366.
Dallas, T., Melbourne, B.A., and Hastings, A. (2019) When can competition and dispersal lead to checkerboard distributions? J Animal Ecol 88: 269-276.
Dearing, J.A., Hannam, J.A., Anderson, A.S., and Wellington, E.M.H. (2001) Magnetic, geochemical and DNA properties of highly magnetic soils in England. Geophys J Int 144: 183-186.
Delgado, M.J., Casella, S., and Bedmar, E.J. (2007) Denitrification in rhizobia-legume symbiosis. In Biology of the Nitrogen Cycle, Bothe, H., Ferguson, S.J., and Newton, W.E. (eds). Amsterdam, The Netherlands: Elsevier, pp. 83-91.
Enwall, K., Throbäck, I.N., Stenberg, M., Söderström, M., and Hallin, S. (2010) Soil resources influence spatial patterns of denitrifying communities at scales compatible with land management. Appl Environ Microbiol 76: 2243-2250.
Etchebehere, C., and Tiedje, J. (2005) Presence of two different active nirS nitrite reductase genes in a denitrifying Thauera sp. from a high-nitrate-removal-rate reactor. Appl Environ Microbiol 71: 5642-5645.
Faust, K., and Raes, J. (2012) Microbial interactions: from networks to models. Nature Rev Microbiol 10: 538-550.
Faust, K., and Raes, J. (2016) CoNet app: inference of biological association networks using Cytoscape [version 2; referees: 2 approved]. F1000Res 5: 1519. https://doi.org/10.12688/f1000research.9050.2.
Faust, K., Sathirapongsasuti, J.F., Izard, J., Segata, N., Gevers, D., Raes, J., and Huttenhower, C. (2012) Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol 8: e1002606.
Fish, J.A., Chai, B., Wang, Q., Sun, Y., Brown, C.T., Tiedje, J.M., and Cole, J.R. (2013) FunGene: the Functional Gene Pipeline and Repository. Front Microbiol 4: 291. https://doi.org/10.3389/fmicb.2013.00291.
Freilich, M.A., Wieters, E., Broitman, B.R., Marquet, P.A., and Navarrete, S.A. (2018) Species co-occurrence networks: can they reveal trophic and non-trophic interactions in ecological communities? Ecology 99: 690-699.
Goberna, M., García, C., Insam, H., Hernández, M.T., and Verdú, M. (2012) Burning fire-prone Mediterranean shrublands: immediate changes in soil microbial community structure and ecosystem functions. Microb Ecol 64: 242-255.
Goberna, M., García, C., and Verdú, M. (2014) A role for biotic filtering in driving phylogenetic clustering in soil bacterial communities. Glob Ecol Biogeogr 23: 1346-1355.
Goberna, M., Navarro-Cano, J.A., and Verdú, M. (2016) Opposing phylogenetic diversity gradients of plant and soil bacterial communities. Proc Roy Soc B 283: 20153003.
Goberna, M., Montesinos, A., Valiente-Banuet, A., Colin, Y., Gómez, A., Donat, S., et al. (2019) Incorporating phylogenetic metrics to microbial co-occurrence networks based on amplicon sequences to discern community assembly processes. Molec Ecol Res 19: 1552-1564.
Goldfarb, K.C., Karaoz, U., Hanson, C.A., Santee, C.A., Bradford, M.A., Treseder, K.K., et al. (2011) Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front Microbiol 2: 94.
Guell, D.C., Brenner, H., Frankel, R.B., and Hartman, H. (1988) Hydrodynamic forces and band formation in swimming magnetotactic bacteria. J Theor Biol 134: 525-542.
Graf, D.R.H., Jones, C.M., and Hallin, S. (2014) Intergenomic comparisons highlight modularity of the denitrification pathway and underpin the importance of community structure for N2O emissions. PLoS ONE 9: e114118.
Hadfield, J.D. (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33: 1-22.
Hallin, S., Jones, C.M., Schloter, M., and Philippot, L. (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3: 597-605.
Hartmann, A., Fu, H., and Burris, R.J. (1986) Regulation of nitrogenase acitivity by ammonium chloride in Azospirillum spp. J Bacteriol 165: 864-870.
HilleRisLambers, J., Adler, P.B., Harpole, W.S., Levine, J.M., and Mayfield, M.M. (2012) Rethinking community assembly through the lens of coexistence theory. Annu Rev Ecol Evol Syst 43: 227-248.
Hooper, D.U., and Johnson, L. (1999) Nitrogen limitation in dryland ecosystems: responses to geographical and temporal variation in precipitation. Biogeochem 46: 247-293.
Hu, H.-W., Chen, D., and He, J.-Z. (2015) Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol Rev 39: 729-749.
Hu, Y., Chen, N., Li, M., Feng, C., and Liu, T. (2019) Insights into simultaneous microbial chromium and nitrate reduction: inhibitory effects and molecular mechanisms. J Chem Technol Biotechnol 94: 2589-2596.
IUSS Working Group WRB. (2006) World reference base for soil resources 2006. World Soil Resources Reports No. 103. FAO, Rome.
Jones, C.M., and Hallin, S. (2010) Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J 4: 633-641.
Jones, C.M., and Hallin, S. (2019) Geospatial variation in co-occurrence networks of nitrifying microbial guilds. Mol Ecol 28: 293-306.
Jones, C.M., Stres, B., Rosenquist, M., and Hallin, S. (2008) Phylogenetic analysis of nitrite, nitric oxide, and nitrous oxide respiratory enzymes reveal a complex evolutionary history for denitrification. Mol Biol Evol 25: 1955-1966.
Jones, C.M., Spor, A., Brennan, F.P., Breuil, M.-C., Bru, D., Lemanceau, P., et al. (2014) Recently identified microbial guild mediates soil N2O sink capacity. Nature Clim Change 4: 801-805.
Klugkist, J., and Haaker, H. (1984) Inhibition of nitrogenase activity by ammonium chloride in Azotobacter vinelandii. J Bacteriol 157: 148-151.
Lerch, T.Z., Chenu, C., Dignac, M.F., Barriuso, E., and Mariotti, A. (2017) Biofilm vs. planktonic lifestyle: consequences for pesticide 2,4-D metabolism by Cupriavidus necator JMP134. Front Microbiol 8: 904. https://doi.org/10.3389/fmicb.2017.00904.
Liu, X., Chen, C.R., Wang, W.J., Hughes, J.M., Lewis, T., Hou, E.Q., and Shen, J. (2013) Soil environmental factors rather than denitrification gene abundance control N2O fluxes in a wet sclerophyll forest with different burning frequency. Soil Biol Biochem 57: 292-300.
Mayfield, M.M., and Levine, J.M. (2010) Opposing effects of competitive exclusion on the phylogenetic structure of the communities. Ecol Lett 13: 1085-1093.
Nadell, C.D., Drescher, K., and Foster, K.R. (2016) Spatial structure, cooperation and competition in biofilms. Nature Rev Microbiol 14: 589-600.
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., et al. (2017). vegan: Community Ecology Package. R package version 2.4-4. https://CRAN.R-project.org/package=vegan
Osvald, M., Maróti, G., Pap, B., and Szanyi, J. (2017) Biofilm forming bacteria during thermal water reinjection. Geofluids 2017: 9231056.
Pascual-García, A., Tamames, J., and Bastolla, U. (2014) Bacteria dialog with Santa Rosalia: are aggregations of cosmopolitan bacteria mainly explained by habitat filtering or by ecological interactions? BMC Microbiol 14: 284.
Pérez-Valera, E., Goberna, M., Faust, K., Raes, J., García, C., and Verdú, M. (2017) Fire modifies the phylogenetic structure of soil bacterial co-occurrence networks. Environ Microbiol 19: 317-327.
Pérez-Valera, E., Verdú, M., Navarro-Cano, J.A., and Goberna, M. (2018) Resilience to fire of phylogenetic diversity across biological domains. Mol Ecol 27: 2896-2908.
Pérez-Valera, E., Goberna, M., and Verdú, M. (2019) Fire modulates ecosystem functioning through the phylogenetic structure of soil bacterial communities. Soil Biol Biochem 129: 80-89.
R Core Team. (2020) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing URL http://www.R-project.org/.
Raymond, J., Siefert, J.L., Staples, C.R., and Blankenship, R.E. (2004) The natural history of nitrogen fixation. Mol Biol Evol 21: 541-554.
Rinaldo, S., and Cutruzzolà, F. (2007) Nitrite reductases in denitrification. In Biology of the Nitrogen Cycle, Bothe, H., Ferguson, S.J., and Newton, W.E. (eds). Amsterdam, The Netherlands: Elsevier, pp. 37-55.
Rinaldo, S., Giardina, G., and Cutruzzolà, F. (2017) Nitrite reductase - cytochrome cd1. In Metalloenzymes in Denitrification: Applications and Environmental impacts, (RSC Metallobiology Series No. 9), Moura, I., Moura, J.J.G., Pauleta, S.R., and Maia, L.B. (eds). London, UK: The Royal Society of Chemistry, pp. 59-90.
Russel, J., Røder, H.L., Madsen, J.S., Burmølle, M., and Sørensen, S.J. (2017) Antagonism correlates with metabolic similarity in diverse bacteria. Proc Natl Acad Sci U S A 114: 10684-10688.
Syakila, A., and Kroeze, C. (2011) The global nitrous oxide budget revisited. Greenh Gas Meas Manag 1: 17-26.
Smith, J., and Ogram, A. (2008) Genetic and functional variation in denitrifier populations along a short-term restoration chronosequences. Appl Environ Microbiol 74: 5615-5620.
Soininen, J., Heino, J., and Wang, J. (2018) A meta-analysis of nestedness and turnover components of beta diversity across organisms and ecosystems. Glob Ecol Biogeogr 27: 96-109.
Tocheva, E.I., Eltis, L.D., and Murphy, M.E.P. (2008) Conserved active site residues limit inhibition of a copper-containing nitrite reductase by small molecules. Biochemistry 47: 4452-4460.
Van Lis, R., Ducluzeau, A.L., Nitschke, W., and Schoepp-Cothenet, B. (2011) The nitrogen cycle in the Archaean: an intricate interplay of enzymatic and abiotic reactions. In Nitrogen Cycling in Bacteria: Molecular Analysis, Moir, J.W.B. (ed). Norwich: Caister Academic Press.
Venables, W.N., and Ripley, B.D. (2002) Modern Applied Statistics with S, 4th ed. New York, USA: Springer.
Wang, Q., Quensen, J.F.I.I.I., Fish, J.A., Lee, T.-K., Sun, Y., Tiedje, J.M., and Cole, J.R. (2013) Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using FrameBot, a new informatics tool. mBio 4: e00592-e00513.
Webb, C.O., Ackerley, D.D., McPeek, M.A., and Donoghue, M.J. (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33: 475-505.
Wittorf, L., Jones, C.M., Bonilla-Rosso, G., and Hallin, S. (2018) Expression of nirK and nirS genes in two strains of Pseudomonas stutzeri harbouring both types of NO-forming nitrite reductases. Res Microbiol 169: 343-347.
Yuan, Q., Liu, P., and Lu, Y. (2012) Differential responses of nirK- and nirS-carrying bacteria to denitrifying conditions in the anoxic rice field soil. Environ Microbiol Rep 4: 113e22.
Zhou, J., Deng, Y., Luo, F., He, Z., Tu, Q., and Zhi, X. (2010) Functional molecular ecological networks. MBio 1: e00169-e00110.
Zumft, W.G. (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61: 533-616.