in

Rainforest-to-pasture conversion stimulates soil methanogenesis across the Brazilian Amazon

  • 1.

    IPCC. Climate change 2013: the Physical Science Basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, et al. editors. Cambridge, United Kingdom and New York, USA: Cambridge University Press; 2013. p. 1535.

  • 2.

    De Azevedo TR, Junior CC, Junior AB, dos Santos Cremer M, Piatto M, Tsai DS, et al. SEEG initiative estimates of Brazilian greenhouse gas emissions from 1970 to 2015. Sci Data. 2018;5:180045.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 3.

    West TAP, Börner J, Fearnside PM. Climatic benefits from the 2006-2017 avoided deforestation in Amazonian Brazil. Front For Glob Change. 2019;2:52.

    Article  Google Scholar 

  • 4.

    Malhi Y, Roberts JT, Betts RA, Killeen TJ, Li W, Nobre CA. Climate change, deforestation, and the fate of the Amazon. Science. 2008;319:169–73.

    CAS  PubMed  Article  Google Scholar 

  • 5.

    Curtis PG, Slay CM, Harris NL, Tyukavina A, Hansen MC. Classifying drivers of global forest loss. Science. 2018;361:1108–11.

    CAS  PubMed  Article  Google Scholar 

  • 6.

    Paula FS, Rodrigues JLM, Zhou J, Wu L, Mueller RC, Mirza BS, et al. Land use change alters functional gene diversity, composition and abundance in Amazon forest soil microbial communities. Mol Ecol. 2014. https://doi.org/10.1111/mec.12786.

  • 7.

    Evans PN, Boyd JA, Leu AO, Woodcroft BJ, Parks DH, Hugenholtz P, et al. An evolving view of methane metabolism in the Archaea. Nat Rev Microbiol. 2019;17:219–32.

    CAS  PubMed  Article  Google Scholar 

  • 8.

    Serrano-Silva N, Sarria-Guzmán Y, Dendooven L, Luna-Guido M. Methanogenesis and methanotrophy in soil: a review. Pedosphere. 2014;24:291–307.

    CAS  Article  Google Scholar 

  • 9.

    Zinder SH. Physiological ecology of methanogens. In: Ferry JG, editor. Methanogenesis: ecology, physiology, biochemistry and genetics. New York, NY, USA: Chapman & Hall; 1993. p. 128–206.

  • 10.

    Schink B, Stams AJM. Syntrophism among prokaryotes. In: Rosenberg E, DeLong F, Lory S, Stackebrandt E, Thompson F, editors. The prokaryotes: prokaryotic communities and ecophysiology. Berlin: Springer; 2013. p. 471–93.

  • 11.

    Costa KC, Leigh JA. Metabolic versatility in methanogens. Curr Opin Biotechnol. 2014;29:70–5.

    CAS  PubMed  Article  Google Scholar 

  • 12.

    Semrau JD, DiSpirito AA, Yoon S. Methanotrophs and copper. FEMS Microbiol Rev. 2010;34:496–531.

    CAS  PubMed  Article  Google Scholar 

  • 13.

    van Teeseling MCF, Pol A, Harhangi HR, van der Zwart S, Jetten MSM, Op den Camp HJM, et al. Expanding the verrucomicrobial methanotrophic world: description of three novel species of Methylacidimicrobium gen. nov. Appl Environ Microbiol. 2014;80:6782–92.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 14.

    Zheng Y, Hou L, Chen F, Zhou J, Liu M, Yin G, et al. Denitrifying anaerobic methane oxidation in intertidal marsh soils: Occurrence and environmental significance. Geoderma. 2020;357:113943.

    CAS  Article  Google Scholar 

  • 15.

    Zheng Y, Wang H, Liu Y, Zhu B, Li J, Yang Y, et al. Methane-dependent mineral reduction by aerobic methanotrophs under hypoxia. Environ Sci Technol Lett. 2020;7:606–12.

    CAS  Article  Google Scholar 

  • 16.

    Murrell JC, Dalton H. Nitrogen fixation in obligate methanotrophs. J Gen Microbiol. 1983;129:3481–6.

    CAS  Google Scholar 

  • 17.

    Graham DW, Chaudhary JA, Hanson RS, Arnold RG. Factors affecting competition between type I and type II methanotrophs in two-organism, continuous-flow reactors. Microb Ecol. 1993;25:1–17.

    CAS  PubMed  Article  Google Scholar 

  • 18.

    Amaral JA, Knowles R. Growth of methanotrophs in methane and oxygen counter gradients. FEMS Microbiol Lett. 1995;126:215–20.

    CAS  Article  Google Scholar 

  • 19.

    Dunfield PF, Liesack W, Henckel T, Knowles R, Conrad R. High-affinity methane oxidation by a soil enrichment culture containing a type II methanotroph. Appl Environ Microbiol. 1999;65:1009–14.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 20.

    Bull ID, Parekh NR, Hall GH, Ineson P, Evershed RP. Detection and classification of atmospheric methane oxidizing bacteria in soil. Nature. 2000;405:175–8.

    CAS  PubMed  Article  Google Scholar 

  • 21.

    Meyer KM, Klein AM, Rodrigues JLM, Nüsslein K, Tringe SG, Mirza BS, et al. Conversion of Amazon rainforest to agriculture alters community traits of methane-cycling organisms. Mol Ecol. 2017;26:1547–56.

    CAS  PubMed  Article  Google Scholar 

  • 22.

    Baani M, Liesack W. Two isoenzymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp. strain SC2. Proc Natl Acad Sci USA. 2008;105:10203–8.

    CAS  PubMed  Article  Google Scholar 

  • 23.

    Sharp CE, Smirnova AV, Graham JM, Stott MB, Khadka R, Moore TR, et al. Distribution and diversity of Verrucomicrobia methanotrophs in geothermal and acidic environments. Environ Microbiol. 2014;16:1867–78.

    CAS  PubMed  Article  Google Scholar 

  • 24.

    Keller M, Goreau TJ, Wofsy SC, Kaplan WA, McElroy MB. Production of nitrous oxide and consumption of methane by forest soils. Geophys Res Lett. 1986;10:1156–9.

    Article  Google Scholar 

  • 25.

    Steudler PA, Melillo JM, Feigl BJ, Neill C, Piccolo MC, Cerri CC. Consequence of forest-to-pasture conversion on CH4 fluxes in the Brazilian Amazon Basin. J Geophys Res Atmos. 1996;101:18547–54.

    CAS  Article  Google Scholar 

  • 26.

    Fearnside PM. Greenhouse gases from deforestation in Brazilian Amazonia: net committed emissions. Climatic Change. 1997;35:321–60.

    CAS  Article  Google Scholar 

  • 27.

    Fernandes SAP, Bernoux M, Cerri CC, Feigl BJ, Piccolo MC. Seasonal variation of soil chemical properties and CO2 and CH4 fluxes in unfertilized and P-fertilized pastures in an Ultisol of the Brazilian Amazon. Geoderma. 2002;107:227–41.

    CAS  Article  Google Scholar 

  • 28.

    Wick B, Veldkamp E, de Mello WZ, Keller M, Crill P. Nitrous oxide fluxes and nitrogen cycling along a pasture chronosequence in Central Amazonia, Brazil. Biogeosciences. 2005;2:175–87.

    CAS  Article  Google Scholar 

  • 29.

    Tveit AT, Urich T, Svenning MM. Metatranscriptomic analysis of active peat soil microbiome. Appl Environ Microbiol. 2014;80:5761–72.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 30.

    Singer E, Wagner M, Woyke T. Capturing the genetic makeup of the active microbiome in situ. ISME J. 2017;11:1949–63.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 31.

    Keiblinger KM, Wilhartitz IC, Schneider T, Roschitzki B, Schmid E, Eberl L, et al. Soil metaproteomics—comparative evaluation of protein extraction protocols. Soil Biol Biochem. 2012;54:14–24.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 32.

    Kroeger ME, Nüsslein K. Stable isotope probing—detection of active microbes in soil. In: Elsas JDV, editor. Modern soil microbiology, 3rd ed. Boca Raton: CRC Press; 2019.

  • 33.

    Esson K, Lin X, Kumaresan D, Chanton JP, Murrell JC, Kostka JE. Alpha- and gammaproteobacterial methanotrophs codominate the active methane-oxidizing communities in an acidic boreal peat bog. Appl Environ Microbiol. 2016;82:2363–71.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 34.

    Dumont MG, Radajewski SM, Miguez CB, McDonald IR, Murrell JC. Identification of a complete methane monooxygenase operon from soil by combining stable isotope probing and metagenomic analysis. Environ Microbiol. 2006;8:1240–50.

    CAS  PubMed  Article  Google Scholar 

  • 35.

    Lu Y, Leuders T, Friedrich MW, Conrad R. Detecting active methanogenic populations on rice roots using stable isotope probing. Environ Microbiol. 2005;7:326–36.

    CAS  PubMed  Article  Google Scholar 

  • 36.

    Neufeld JD, Vohra J, Dumont MG, Lueders T, Manefield M, Friedrich MW, et al. DNA stable-isotope probing. Nat Protoc. 2007;2:860–6.

    CAS  PubMed  Article  Google Scholar 

  • 37.

    Holmes AJ, Costello A, Lidstrom ME, Murrell JC. Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett. 1995;132:203–8.

    CAS  PubMed  Article  Google Scholar 

  • 38.

    Costello A, Lidstrom ME. Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 1999;65:5066–74.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 39.

    Steinberg LM, Regan JM. Phylogenetic comparison of the methanogenic communities from an acidic, oligotrophic fen and an anaerobic digester treating municipal wastewater sludge. Appl Environ Microbiol. 2008;74:6663–71.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 40.

    Meyer KM, Morris AH, Webster K, Klein AM, Kroeger ME, Meredith LK, et al. Belowground changes to community structure alter methane-cycling dynamics in Amazonia. 2020. https://www.biorxiv.org/content/10.1101/2020.03.10.984807v1. in review.

  • 41.

    Navarrete AA, Tsai SM, Mendes LW, Faust K, de Hollander M, Cassman NA, et al. Soil microbiome responses to the short-term effects of Amazonian deforestation. Mol Ecol. 2015;24:2433–48.

    CAS  PubMed  Article  Google Scholar 

  • 42.

    Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 43.

    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  PubMed Central  Article  Google Scholar 

  • 44.

    Keegan KP, Glass EM, Meyer F. MG-RAST, a metagenomics service for analysis of microbial community structure and function. Methods Mol Biol. 2016;1399:207–33.

    CAS  PubMed  Article  Google Scholar 

  • 45.

    R Core Team. R: a language and environment for statistical computing. Vienna Austria: R Foundation for Statistical Computing; 2018. https://www.r-project.org/.

  • 46.

    Oksanen JF, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: community ecology package. R package version. 2018;2:4–6. https://CRAN.R-project.org/package=vegan.

  • 47.

    Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014;30:3123–4.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 48.

    Wickham H. ggplot2: elegant graphics for data analysis. New York: Spring-Verlag; 2016.

    Google Scholar 

  • 49.

    Parks DH, Tyson GW, Hugenholtz P, Beiko RG. STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics. 2014;30:3123–4.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 50.

    Pinto AJ, Raskin L. PCR biases distort bacterial and archaeal community structure in pyrosequencing datasets. PLoS ONE. 2012;7:e43093.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 51.

    Huse SM, Welch DM, Morrison HG, Sogin ML. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol. 2010;12:1889–98.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 52.

    Quince C, Walker AW, Simpson JT, Loman NJ, Segata N. Shotgun metagenomics, from sampling to sequencing and analysis. Nat Biotechnol. 2017;35:833–44.

    CAS  PubMed  Article  Google Scholar 

  • 53.

    Coyotzi S, Pratscher J, Murrell JC, Neufeld JD. Targeted metagenomics of active microbial populations with stable-isotope probing. Curr Opin Biotechnol. 2016;41:1–8.

    CAS  PubMed  Article  Google Scholar 

  • 54.

    Eyice Ö, Namura M, Chen Y, Mead A, Samavedam S, Schäfer H. SIP metagenomics identifies uncultivated Methylophilaceae as dimethylsulphide degrading bacteria in soil and lake sediment. Int Soc Microb Ecol J. 2015;9:2336.

    CAS  Google Scholar 

  • 55.

    Cardoso D, Sarkinen T, Alexander S, Amorim AM, Bittrich V, Celis M, et al. Amazon plant diversity revealed by a taxonomically verified species list. Proc Natl Acad Sci USA. 2017;114:10695–700.

    CAS  PubMed  Article  Google Scholar 

  • 56.

    Sgouridis F, Ullah S. Soil greenhouse gas fluxes, environmental controls, and the partitioning of N2O sources in UK natural and seminatural land use types. J Geophys Res Biogeosciences. 2017. https://doi.org/10.1002/2017JG003783.

  • 57.

    Wanyama I, Pelster DE, Butterbach-Bahl K, Verchot LV, Martius C, Rufino MC. Soil carbon dioxide and methane fluxes from forests and other land use types in an African tropical montane region. Biogeochemistry. 2019;143:171–90.

    CAS  Article  Google Scholar 

  • 58.

    Lackner N, Hintersonnleitner A, Wagner AO, Illmer P. Hydrogenotrophic methanogenesis and autotrophic growth of Methanosarcina thermophila. Archaea. 2018;2018:4712608.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 59.

    Ferry JG. Fundamentals of methanogenic pathways that are key to the biomethanation of complex biomass. Curr Opin Biotechnol. 2011;22:351–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 60.

    Welander PV, Metcalf WW. Loss of the mtr operon in Methanosarcina blocks growth on methanol, but not methanogenesis, and reveals an unknown methanogenic pathway. Proc Natl Acad Sci USA. 2005;102:10664–9.

    CAS  PubMed  Article  Google Scholar 

  • 61.

    Mand TD, Metcalf WW. Energy conservation and hydrogenase function in methanogenic archaea, in particular the genus Methanosarcina. Microbiol Mol Biol Rev. 2019;83:e00020–19.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 62.

    Lammel DR, Feigl BJ, Cerri CC, Nusslein K. Specific microbial gene abundances and soil parameters contribute to C, N, and greenhouse gas process rates after land use change in Southern Amazonian Soils. Front Microbiol. 2015;6:1057.

    PubMed  PubMed Central  Article  Google Scholar 

  • 63.

    Kroeger ME, Delmont TO, Meyer KM, Guo J, Khan K, Rodrigues JLM, et al. New biological insights into how deforestation in Amazonia affects soil microbial communities using metagenomics and metagenome-assembled genomes. Front Microbiol. 2018;9:1635.

    PubMed  PubMed Central  Article  Google Scholar 

  • 64.

    Pedrinho A, Mendes LW, Merloti LF, de Cassia da Fonseca M, de Souza Cannavan F, Tsai SM. Forest-to-pasture conversion and recovery based on assessment of microbial communities in Eastern Amazon rainforest. FEMS Microbiol Ecol. 2019;95:fiy236.

    CAS  PubMed  Article  Google Scholar 

  • 65.

    Carini P, Marsden PJ, Leff JW, Morgan EE, Strickland MS, Fierer N. Relic DNA is abundant in soil and obscures estimates of soil microbial diversity. Nat Microbiol. 2017;2:16242.

    CAS  Article  Google Scholar 

  • 66.

    Lennon JT, Muscarella ME, Placella SA, Lehmkuhl BK. How, when, and where relic DNA affects microbial diversity. MBio. 2018;9:e00637–18.

    PubMed  PubMed Central  Google Scholar 

  • 67.

    Sirois SH, Buckley DH. Factors governing extracellular DNA degradation dynamics in soil. Environ Microbiol Rep. 2019;11:173–84.

    CAS  PubMed  Article  Google Scholar 

  • 68.

    Mancinelli RL. The regulation of methane oxidation in soil. Annu Rev Microbiol. 1995;49:581–605.

    CAS  PubMed  Article  Google Scholar 

  • 69.

    Guggenheim C, Brand A, Bürgmann H, Sigg L, Wehrli B. Aerobic methane oxidation under copper scarcity in a stratified lake. Sci Rep. 2019;9:4817.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 70.

    Knapp CW, Fowle DA, Kulczycki E, Roberts JA, Graham DW. Methane monooxygenase gene expression mediated by methanobactin in the presence of mineral copper sources. Proc Natl Acad Sci USA. 2007;104:12040–5.

    CAS  PubMed  Article  Google Scholar 

  • 71.

    Rodrigues JLM, Pellizari VH, Mueller R, Baek K, da C Jesus E, Paula FS, et al. Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc Natl Acad Sci USA. 2013;110:988–93.

    CAS  PubMed  Article  Google Scholar 

  • 72.

    Hoehler T, Gunsalus RP, McInerney MJ. Environmental Constraints that Limit Methanogenesis. In Timmis KN, editor. Handbook of Hydrocarbon and Lipid Microbiology. Berlin, Heidelberg: Springer; 2010. p. 635–54.

  • 73.

    Elshahed MS, Bhupathiraju VK, Wofford NQ, Nanny MA, McInerney MJ. Metabolism of benzoate, cyclohex-1-ene carboxylate, and cyclohexane carboxylate by “Syntrophus aciditrophicus” strain SB in syntrophic association with H2-using microorganisms. Appl Environ Microbiol. 2001;67:1728–38.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 74.

    Zehnder AJB, Stumm W. Geochemistry and biogeochemistry of anaerobic habitats. In Zehnder AJB editor. Biology of Anaerobic Microorganisms. New York, NY, USA: John Wiley & Sons; 1988. p. 1–38.

  • 75.

    Wolfe RS. My kind of biology. Annu Rev Microbiol. 1991;45:1–35.

    CAS  PubMed  Article  Google Scholar 

  • 76.

    Strittmatter AW, Liesegang H, Rabus R, Decker I, Amann J, Andres S, et al. Genome sequence of Desulfobacterium autotrophicum HRM2, a marine sulfate reducer oxidizing organic carbon completely to carbon dioxide. Environ Microbiol. 2009;11:1038–55.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 77.

    Badziong W, Ditter B, Thauer RK. Acetate and carbon dioxide assimilation by Desulfovibrio vulgaris (Marburg), growing on hydrogen and sulfate as sole energy source. Arch Microbiol. 1979;123:301–5.

    CAS  Article  Google Scholar 

  • 78.

    Watson SW, Waterbury JB. Characteristics of two marine nitrite oxidizing bacteria, Nitrospina gracilis nov. gen. nov. sp. and Nitrococcus mobilis nov. gen. nov. sp. Arch Microbiol. 1971;77:203–30.

    Google Scholar 

  • 79.

    Sorokin DY, Tourova TP, Lysenko AM, Mityushina LL, Kuenen JG. Thioalkalivibrio thiocyanoxidans sp. nov. and Thioalkalivibrio paradoxus sp. nov., novel alkaliphilic, obligately autotrophic, sulfur-oxidizing bacteria capable growth on thiocyanate, from soda lakes. IJSEM. 2002;52:657–64.

    CAS  PubMed  Google Scholar 

  • 80.

    Kukla J, Whitfeld T, Cajthaml T, Baldrian P, Veselá-Šimáčková H, Novotný V, et al. The effect of traditional slash-and-burn agriculture on soil organic matter, nutrient content, and microbiota in tropical ecosystems of Papua New Guinea. Land Degrad Dev. 2018;30:166–77.

    Article  Google Scholar 

  • 81.

    Banat IM, Marchant R. Geobacillus activities in soil and oil contamination remediation. In: Logan NA, De Vos P, editors. Endospore-forming soil bacteria, soil biology 27, Berlin Heidelberg: Springer-Verlag; 2011. p. 259–70.

  • 82.

    Durrer A, Margenot AJ, Silva LCR, Bohannan BJM, Nüsslein K, van Haren J, et al. Beyond total carbon: long-term effect of deforestation on Amazonian soils. Biogeochemistry BIOG-D-19-00139. in review.

  • 83.

    Nazina TN, Tourova TP, Poltaraus AB, Novikova EV, Grigoryan AA, Ivanova AE, et al. Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subterraneus gen. nov., sp. nov. and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus thermoleovorans, Bacillus kaustophilus, Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G.th. IJSEM. 2001;51:433–46.

    CAS  PubMed  Google Scholar 

  • 84.

    Schnürer A, Schink B, Svensson BH. Clostridium ultunense sp. nov., a mesophilic bacterium oxidizing acetate in syntrophic association with a hydrogenotrophic methanogenic bacterium. IJSEM. 1996;46:1145–52.

    Google Scholar 

  • 85.

    Myhr S, Torsvik T. Denitrovibrio acetiphilus, a novel genus and species of dissimilatory nitrate-reducing bacterium isolated from an oil reservoir model column. IJSEM. 2000;50:1611–9.

    CAS  PubMed  Google Scholar 

  • 86.

    Yao H, Conrad R, Wassmann R, Neue HU. Effect of soil characteristics on sequential reduction and methane production in sixteen rice paddy soils from Chine, the Philippines, and Italy. Biogeochemistry. 1999;47:269–95.

    CAS  Article  Google Scholar 

  • 87.

    Achtnich C, Bak F, Conrad R. Competition for electron donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biol Fertil Soils. 1995;19:65–72.

    CAS  Article  Google Scholar 

  • 88.

    Verchot LV, Davidson EA, Cattânio JH, Ackerman IL. Land-use change and biogeochemical controls of methane fluxes in soils of Eastern Amazonia. Ecosystems. 2000;3:41–56.

    CAS  Article  Google Scholar 

  • 89.

    Wagner R, Zona D, Oechel W, Lipson D. Microbial community structure and soil pH correspond to methane production in Arctic Alaska soils. Environ Microbiol. 2017;19:3398–410.

    CAS  PubMed  Article  Google Scholar 

  • 90.

    Feigl BJ, Melillo J, Cerri CC. Changes in the origin and quality of soil organic matter after pasture introduction in Rôndonia (Brazil). Plant Soil. 1995;175:21–9.

    CAS  Article  Google Scholar 

  • 91.

    Salimon CI, Davidson EA, Victoria RL, Melo AWF. CO2 flux from soil in pastures and forests in southwestern Amazonia. Glob Change Biol. 2004;10:833–43.

    Article  Google Scholar 

  • 92.

    Wilhelm RC, Singh R, Eltis LD, Mohn WW. Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing. ISME J. 2019;13:413–8.

    CAS  PubMed  Article  Google Scholar 

  • 93.

    Pepe-Ranney C, Campbell AN, Koechli CN, Berthrong S, Buckley DH. Unearthing the ecology of soil microorganisms using a high-resolution DNA-SIP approach to explore cellulose and xylose metabolism in soil. Front Microbiol. 2016;7:703.

    PubMed  PubMed Central  Article  Google Scholar 

  • 94.

    Murase J, Hordijk K, Tayasu I, Bodelier PLE. Strain-specific incorporation of methanotrophic biomass into eukaryotic grazers in a rice field soil revealed by PLFA-SIP. FEMS Microbiol Ecol. 2011;75:284–90.

    CAS  PubMed  Article  Google Scholar 

  • 95.

    Radajewski S, Ineson P, Parekh NR, Murrell JC. Stable-isotope probing as a tool in microbial ecology. Nature. 2000;403:646–9.

    CAS  PubMed  Article  Google Scholar 

  • 96.

    Cébron A, Bodrossy L, Chen Y, Singer AC, Thompson IP, Prosser JI, et al. Identity of active methanotrophs in landfill cover soil as revealed by DNA-stable isotope probing. FEMS Microbiol Ecol. 2007;62:12–23.

    PubMed  Article  CAS  Google Scholar 

  • 97.

    Mathew RP, Feng Y, Githinji L, Ankumah R, Balkcom KS. Impact of no-tillage and conventional tillage systems on soil microbial communities. Appl Environ Soil Sci. 2012;2012:548620.

    Article  Google Scholar 

  • 98.

    Eilers KG, Debenport S, Anderson S, Fierer N. Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biol Biochem. 2012;50:58–65.

    CAS  Article  Google Scholar 

  • 99.

    Zhou J, Wu L, Deng Y, Zhi X, Jiang Y-H, Tu Q, et al. Reproducibility and quantitation of amplicon sequencing-based detection. ISME J. 2011;5:1303–13.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 100.

    Wen C, Wu L, Qin Y, Van Nostrand JD, Ning D, Sun B, et al. Evaluation of the reproducibility of amplicon sequencing with Illumina MiSeq platform. PLoS ONE. 2017. https://doi.org/10.1371/journal.pone.0176716.

  • 101.

    Berenguer E, Gardner TA, Ferreira J, Aragao LE, Camargo PB, Cerri CE, et al. Developing cost-effective field assessments of carbon stocks in human-modified tropical forests. PLoS ONE. 2015;10:e0133139.

    PubMed  PubMed Central  Article  CAS  Google Scholar 


  • Source: Ecology - nature.com

    More than a meal

    Linking structural and compositional changes in archaeological human bone collagen: an FTIR-ATR approach