Abstract
Here we use a top-down and bottom-up approach in landscape ecology to analyze the active microbes processing methane fluxes (FCH4) in seasonally flooded-forest (FOR) and -traditional farming systems (TFS) in Amazonian floodplains flooded with black, white, and clear water. Our results revealed higher CH4 emissions from water-atmosphere interface in clear water floodplain, followed by black and white water floodplain, respectively. Active methanogenic and methanotrophic taxa were ubiquitous at 0–15 and 15–30 cm soil layer in FOR and TFS, with differences among the water types with respect to the richness, evenness and diversity of the methanogenic communities. These ecological results were not generalizable regarding to FOR and TFS sites, soil layers, and non-flooded and flooded periods. Despite the predominant oxidation of CH4 in the non-flooded period, higher richness and diversity of methanotrophs were revealed for FOR and TFS in the flooded period. In turn, the structure of the methanogenic and methanotrophic communities and their variation were influenced mainly by soil physicochemical factors, water type, soil depth and the presence of nitrifiers, as Nitrososphaera and Nitrospira. Our study reveals a signature across methanotrophic communities in soils from Amazon floodplain with different water types, with a putative disproportionate role of NC10 phylum in CH4 mitigation in natural and agricultural Amazonian floodplains. These findings open the possibilities to explore the role of NC10 phylum in the carbon cycling in Amazon.
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References
Amaral JHF, Farjalla VF, Melack JM, Kasper D, Scofield V, Barbosa PM, Forsberg BR (2019) Seasonal and spatial variability of CO2 in aquatic environments of the central lowland Amazon basin. Biogeochemistry 143:133–149. https://doi.org/10.1007/s10533-019-00554-9
Anderson I, Ulrich LE, Lupa B, Susanti D, Porat I, Hooper SD et al (2009) Genomic characterization of methanomicrobiales reveals three classes of methanogens. PLoS ONE 4:e5797. https://doi.org/10.1371/journal.pone.0005797
Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847–862. https://doi.org/10.1038/ismej.2011.141
Angle JC, Morin TH, Solden LM, Narrowe AB, Smith GJ, Borton MA et al (2017) Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions. Nat Commun 8:1–9. https://doi.org/10.1038/s41467-017-01753-4
Apprill A, Mcnally S, Parsons R, Weber L (2015) Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Micro Ecol 75:129–137. https://doi.org/10.3354/ame01753
Arshad A, Speth DR, De Graaf RM, Op den Camp HJM, Jetten MSM, Welte CU (2015) A metagenomics-based metabolic model of nitrate-dependent anaerobic oxidation of methane by Methanoperedens-like Archaea. Front Microbiol 6:1–14. https://doi.org/10.3389/fmicb.2015.01423
Barbosa PM, Melack JM, Farjalla VF, Amaral JHF, Scofield V, Forsberg BR (2016) Diffusive methane fluxes from Negro, Solimões and Madeira rivers and fringing lakes in the Amazon basin. Limnol Oceanogr 61:S221-237. https://doi.org/10.1002/lno.10358
Barbosa PM, Farjalla VF, Melack JM, Amaral JHF, da Silva JS, Forsberg BR (2018) High rates of methane oxidation in an Amazon floodplain lake. Biogeochemistry 137:351–365. https://doi.org/10.1007/s10533-018-0425-2
Barbosa PM, Melack JM, Amaral JHF, MacIntyre S, Kasper D, Cortés A et al (2020) Dissolved methane concentrations and fluxes to the atmosphere from a tropical floodplain lake. Biogeochemistry 148:129–151. https://doi.org/10.1007/s10533-020-00650-1
Barrios E, Sileshi GW, Shepherd K, Sinclair F (2012) Agroforestry and soil health: linking trees, soil biota, and ecosystem services. In: Wall DH, Bardgett RD, Behan-Pelletier V, Herrick JE, Jones TH, Ritz K et al (eds) Soil ecology and ecosystem services. Oxford University Press, Oxford, pp 315–330
Bartlett RJ, James BR (1993) Química redox do solo. Adv Agron 50:151–208
Bastviken D, Tranvik LJ, Downing JA, Crill PM, Enrich-Prast A (2011) Freshwater methane emissions offset the continental carbon sink. Science 331(6013):50: https://doi.org/10.1126/science.1196808
Beaulieu JJ, DelSontro T, Downing JA (2019) Eutrophication will increase methane emissions from lakes and impoundments during the 21st century. Nat Commun 10:3–7. https://doi.org/10.1038/s41467-019-09100-5
Bodelier PLE, Laanbroek HJ (2004) Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiol Ecol 47:265–277. https://doi.org/10.1016/S0168-6496(03)00304-0
Borcard D et al (2011) Canonical ordination. Num Ecol R. https://doi.org/10.1007/978-1-4419-7976-6
Browne P, Tamaki H, Kyrpides N, Woyke T, Goodwin L, Imachi H et al (2017) Genomic composition and dynamics among Methanomicrobiales predict adaptation to contrasting environments. ISME J 11:87–99. https://doi.org/10.1038/ismej.2016.104
Camargo FAO, Santos GA, Zonta E (1999) Alterações eletro-química em solos inundados. Ciência Rural 29:171–180. https://doi.org/10.1590/S0103-84781999000100032
Camargo OA, Moniz AC, Jorge JA, Valadares JMA (2009) Métodos de análise química, mineralógica e física de solos do Instituto Agronômico de Campinas. Boletim Técnico, 106, 77. Campinas: Instituto Agronômico.
Cantarella H, Prochnow LI (2001) Determinação de sulfato em solos. In: Raij B Van, Andrade JC, Cantarella HC, Quaggio JA (eds). Análise Química para Avaliação da Fertilidade de Solos Tropicais. Campinas: Instituto Agronômico de Campinas, pp 225–230.
Caporaso JG, Bittinger K, Bushman FD, Desantis TZ, Andersen GL, Knight R (2010a) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267. https://doi.org/10.1093/bioinformatics/btp636
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010b) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Catalán N, Kellerman AM, Peter H, Carmona F, Tranvik LJ (2015) Absence of a priming effect on dissolved organic carbon degradation in lake water. Limnol Oceanog 60:159–168. https://doi.org/10.1002/lno.10016
Cole JJ, Prairie YT, Caraco NF, McDowell WH, Tranvik LJ, Striegl RG et al (2007) Plumbing the global carbon cycle: Integrating inland waters into the terrestrial carbon budget. Ecosystems 10:171–184. https://doi.org/10.1007/s10021-006-9013-8
Conrad R, Klose M, Claus P, Enrich-Prast A (2010) Methanogenic pathway, 13C isotope fractionation, and archaeal community composition in the sediment of two clear-water lakes of Amazonia. Limnol Oceanogr 55:689–702. https://doi.org/10.4319/lo.2009.55.2.0689
Conrad R, Noll M, Claus P, Klose M, Bastos WR, Enrich-Prast A (2011) Stable carbon isotope discrimination and microbiology of methane formation in tropical anoxic lake sediments. Biogeosciences 8:795–814. https://doi.org/10.5194/bg-8-795-2011
Conrad R, Ji Y, Noll M, Klose M, Claus P, Enrich-Prast A (2014) Response of the methanogenic microbial communities in Amazonian oxbow lake sediments to desiccation stress. Environ Microbiol 16:1682–1694. https://doi.org/10.1111/1462-2920.12267
Cui M, Ma A, Qi H, Zhuang X, Zhuang G (2015) Anaerobic oxidation of methane: An “active” microbial process. Microbiologyopen 4:1–11. https://doi.org/10.1002/mbo3.232
Dalmagro HJ, Zanella de Arruda PH, Vourlitis GL, Lathuillière MJ, de Nogueira J, Couto EG, Johnson MS (2019) Radiative forcing of methane fluxes offsets net carbon dioxide uptake for a tropical flooded forest. Glob Chang Biol 25:1967–1981. https://doi.org/10.1111/gcb.14615
Devol AH, Richey JE, Clark WA, King SL, Martinelli LA (1988) Methane emissions to the troposphere from the Amazon floodplain. J Geophys Res Atmos 93:1583–1592. https://doi.org/10.1029/JD093iD02p01583
Devol AH, Richey JE, Forsberg BR, Martinelli LA (1990) Seasonal dynamics in methane emissions from the Amazon River floodplain to the troposphere. J Geophys Res Atmos 95:16417–16426. https://doi.org/10.1029/JD095iD10p16417
Devol AH, Richey JE, Forsberg BR, Martinelli LA (1994) Environmental methane in the Amazon River floodplain. In: Mitsch WJ (ed) Global wetlands: old world and new. Elsevier Science, Amsterdam, pp 151–165
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
EMBRAPA 2009. Manual de Análises Químicas de Solos, Plantas e Fertilizantes. 2ª Ed rev. Brasília, BR: EMBRAPA Informação Tecnológica
Erkel C, Kube M, Reinhardt R, Liesack W (2006) Genome of Rice Cluster I Archaea - the key methane producers in the rice rhizosphere. Science 313:370–372. https://doi.org/10.1126/science.1127062
Ettwig KF, Shima S, Van de Pas-Schoonen KT, Kahnt J, Medema MH, Op den Camp HJ et al (2008) Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ Microbiol 10:3164–3173. https://doi.org/10.1111/j.1462-2920.2008.01724.x
Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MMM et al (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548. https://doi.org/10.1038/nature08883
Evans PN, Boyd JA, Leu AO, Woodcroft BJ, Parks DH, Hugenholtz P, Tyson GW (2019) An evolving view of methane metabolism in the Archaea. Nat Rev Microbiol. https://doi.org/10.1038/s41579-018-0136-7
Furch K, Junk WJ (1997) Physicochemical conditions in the floodplains. In: Junk WJ (ed) Central Amazon floodplain: ecological studies. Springer, Berlin, pp 69–107
Gabriel GVM, Oliveira LC, Barros DJ, Bento MS, Neu V, Toppa RH et al (2020) Methane emission suppression in flooded soil from Amazonia. Chemosphere 250:1–10. https://doi.org/10.1016/j.chemosphere.2020.126263
Gontijo JB, Paula FS, Venturini AM, Yoshiuraa CA, Borges CD, Moura JMS, Bohannan BJM et al (2021) Not just a methane source: Amazonian floodplain sediments harbour a high diversity of methanotrophs with different metabolic capabilities. Mol Ecol. https://doi.org/10.1111/mec.15912
Graf JS, Mayr MJ, Marchant HK, Tienken D, Hach PF, Brand A et al (2018) Bloom of a denitrifying methanotroph, “Candidatus Methylomirabilis Limnetica”, in a deep stratified lake. Environ Microbiol 20:2598–2614. https://doi.org/10.1111/1462-2920.14285
Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27. https://doi.org/10.1038/ismej.2009.97
Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P et al (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500:567–570. https://doi.org/10.1038/nature12375
Harriss R, Sebacher D, Day F (1982) Methane flux in the Great Dismal Swamp. Nature 297:673–674. https://doi.org/10.1038/297673a0
He Z, Geng S, Cai C, Liu S, Liu Y, Pan Y et al (2015) Anaerobic oxidation of methane coupled to nitrite reduction by halophilic marine NC10 bacteria. Appl Environ Microbiol 81:5538–5545. https://doi.org/10.1128/AEM.00984-15
Hernández M, Conrad R, Klose M, Ma K, Lu Y (2017) Structure and function of methanogenic microbial communities in soils from flooded rice and upland soybean fields from Sanjiang Plain, NE China. Soil Biol Biochem 105:81–91. https://doi.org/10.1016/j.soilbio.2016.11.010
Hess LL, Melack JM, Affonso AG, Barbosa C, Gastil-Buhl M, Novo EMLM (2015) Wetlands of the lowland Amazon basin: extent, vegetative cover, and dual-season inundated area as mapped with JERS-1 synthetic aperture radar. Wetlands 35:745–756. https://doi.org/10.1007/s13157-015-0666-y
Hofmann K, Praeg N, Mutschlechner M, Wagner AO, Illmer P (2016) Abundance and potential metabolic activity of methanogens in well-aerated forest and grassland soils of an alpine region. FEMS Microbiol Ecol 92:fiv171. https://doi.org/10.1093/femsec/fiv171
Ji Y, Angel R, Klose M, Claus P, Marotta H, Pinho L et al (2016) Structure and function of methanogenic microbial communities in sediments of Amazonian lakes with different water types. Environ Microbiol 18:5082–5100. https://doi.org/10.1111/1462-2920.13491
Keller M, Mitre ME, Stallard RF (1990) Consumption of atmospheric methane in soils of central Panama: effects of agricultural development. Global Biogeochem Cycles 4:21–27. https://doi.org/10.1029/GB004i001p00021
Kits KD, Campbell DJ, Rosana AR, Stein LY (2015) Diverse electron sources support denitrification under hypoxia in the obligate methanotroph Methylomicrobium album strain BG8. Front Microbiol 6:1–11. https://doi.org/10.3389/fmicb.2015.01072
Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M et al (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:1–11. https://doi.org/10.1093/nar/gks808
Knittel K, Boetius A (2009) Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol 63:311–334. https://doi.org/10.1146/annurev.micro.61.080706.093130
Kravchenko I, Sukhacheva M, Menko E, Sirin A (2014) Anaerobic nitrite-dependent methane-oxidizing bacteria - novel participants in methane cycling of drained peatlands ecosystems. In: EGU General Assembly Conference, abstracts 8242
Krom MD (1980) Spectrophotometric determination of ammonia: a study of a modified Berthelot reaction using salicylate and dichloroisocyanurate. Analyst 105:305–316. https://doi.org/10.1039/AN9800500305
Krzycki JA, Kenealy WR, Deniro MJ, Zeikus JG (1987) Stable carbon isotope fractionation by methanosarcina barkeri during methanogenesis from acetate, methanol, or carbon dioxide-hydrogen. Appl Environ Microbiol 53:2597–2599
Lozupone C, Hamady M, Knight R (2006) UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinform 7:1–14. https://doi.org/10.1186/1471-2105-7-371
Marengo JA, Liebmann B, Grimm AM, Misra V, Silva Dias PL, Cavalcanti IFA et al (2012) Recent developments on the South American monsoon system. Int J Climatol 32:1–21. https://doi.org/10.1002/joc.2254
Melack JM (2016) Aquatic ecosystems. In: Nagy L, Forsberg B, Artaxo P (eds) Interactions between biosphere, atmosphere and human land use in the Amazon Basin. Springer, Berlin, pp 119–148
Nazaries L, Pan Y, Bodrossy L, Baggs EM, Millard P, Murrell JC et al (2013) Microbial regulation of biogeochemical cycles: evidence from a study on methane flux and land-use change. Appl Environ Microbiol 79:4031–4040. https://doi.org/10.1128/AEM.00095-13
Neuwirth E (2014) Package ‘RColorBrewer’. https://cran.r-project.org/web/packages/RColorBrewer/RColorBrewer.pdf
Norman RJ, Edberg JC, Stucki JW (1985) Determination of nitrate in soil extracts by dual-wavelength ultraviolet spectrophotometry. Soil Sci Soc Am J 49:1182–1185. https://doi.org/10.2136/sssaj1985.03615995004900050022x
Oksanen J, Blanchet FG, Legendre P, Minchin PR, O’Hara RB, Simpson GL et al (2016) Vegan: community ecology package R package version 2.3-3
Oswald K, Graf J, Littmann S, Tienken D, Brand A, Wehrli B et al (2017) Crenothrix are major methane consumers in stratified lakes. ISME J 11:2124–2140. https://doi.org/10.1038/ismej.2017.77
Padilla C, Bristow L, Sarode N, Garcia-Robledo E, Gómez Ramírez E, Benson CR et al (2016) NC10 bacteria in marine oxygen minimum zones. ISME J 10:2067–2071. https://doi.org/10.1038/ismej.2015.262
Pan Y, Abell GCJ, Bodelier PLE, Meima-Franke M, Sessitsch A, Bodrossy L (2014) Remarkable recovery and colonization behaviour of methane oxidizing bacteria in soil after disturbance is controlled by methane source only. Microb Ecol 68:259–270. https://doi.org/10.1007/s00248-014-0402-9
Pangala SR, Enrich-Prast A, Basso LS, Peixoto RB, Bastviken D, Hornibrook ERC et al (2017) Large emissions from floodplain trees close the Amazon methane budget. Nature 552:230–234. https://doi.org/10.1038/nature24639
Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 18:1403–1414. https://doi.org/10.1111/1462-2920.13023
Ploner A (2014) Heatplus: heatmaps with row and/or column covariates and colored clusters. R package version 2.12.0
Pylro VS, Roesch LF, Morais DK, Clark IM, Hirsch PR, Tótola MR (2014) Data analysis for 16S microbial profiling from different benchtop sequencing platforms. J Microbiol Methods 107:30–37. https://doi.org/10.1016/j.mimet.2014.08.018
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Raghoebarsing AA, Pol A, Van de Pas-Schoonen KT, Smolders AJ, Ettwig KF, Rijpstra WI et al (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440:918–921. https://doi.org/10.1038/nature04617
Richey JE, Hedges JE, Devol AH, Quay PD, Victoria LA, Martinelli LA et al (1990) Biogeochemistry of carbon in the Amazon River. Limnol Oceanogr 35:352–371. https://doi.org/10.4319/lo.1990.35.2.0352
Ringeval B, Houweling S, Van Bodegom PM, Spahni R, Van Beek R, Joos F, Röckmann T (2014) Methane emissions from floodplains in the Amazon Basin: challenges in develo** a process-based model for global applications. Biogeosciences 11:1519–1558. https://doi.org/10.5194/bg-11-1519-2014
Ríos-Villamizar EA, Piedade MTF, Da Costa JG, Adeney JM, Junk WJ (2013) Chemistry of different Amazonian water types for river classification: a preliminary review. WIT Trans Ecol Environ 178:17–28
Salati E, Dall’Olio A, Matsui E, Gat JR (1979) Recycling of water in the Amazon Basin: an isotopic study. Water Resour Res 15:1250–1258. https://doi.org/10.1029/WR015i005p01250
Satinsky BM, Fortunato CS, Doherty M, Smith CB, Sharma S, Ward ND et al (2015) Metagenomic and metatranscriptomic inventories of the lower Amazon River, May 2011. Microbiome 3:1–8. https://doi.org/10.1186/s40168-015-0099-0
Sawakuchi HO, Bastviken D, Sawakuchi AO, Krusche AV, Ballester MVR, Richey JE (2014) Methane emissions from Amazonian Rivers and their contribution to the global methane budget. Glob Chang Biol 20:2829–2840. https://doi.org/10.1111/gcb.12646
Sawakuchi HO, Bastviken D, Sawakuchi AO, Ward ND, Borges CD, Tsai SM et al (2016) Oxidative mitigation of aquatic methane emissions in large Amazonian rivers. Glob Change Biol 22:1075–1085. https://doi.org/10.1111/gcb.13169
Scheller S, Ermler U, Shima S (2020) Catabolic pathways and enzymes involved in anaerobic methane oxidation. In: Boll M (ed) Anaerobic utilization of hydrocarbons, oils, and lipids handbook of hydrocarbon and lipid microbiology. Springer, Cham, pp 31–59
Schmidt T, Schaechter M (2009) Topics in ecological and environmental microbiology. Academic Press, San Diego
Schwartz G, Ferreira MD, Lopes JD (2015) Silvicultural intensification and agroforestry systems in secondary tropical forests: a review. Revista De Ciências Agrárias 58:319–326. https://doi.org/10.4322/rca.1830
Segarra KEA, Schubotz F, Samarkin V, Yoshinaga MY, Hinrichs KU, Joye SB (2015) High rates of anaerobic methane oxidation in freshwater wetlands reduce potential atmospheric methane emissions. Nat Commun 6:2–9. https://doi.org/10.1038/ncomms8477
Shen LD, Wu HS, Gao ZQ, Liu X, Li J (2016) Comparison of community structures of candidatus methylomirabilis oxyfera-like bacteria of NC10 phylum in different freshwater habitats. Sci Rep 6:25647. https://doi.org/10.1038/srep25647
Sioli H (1950) Das Wasser in Amazonasgebiet. Fosch, Fortschr, 274–180.
Sioli H (1955) Beiträge zur regionalen Limnologie des Amazonasgebietes. III. Über einige Gewässer des oberen Rio Negro-Gebietes. Arch Hydrobiol 50:1–32
Sippel SJ, Hamilton SK, Melack JM (1992) Inundation area and morphometry of lakes on the Amazon River floodplain, Brazil. Arch Hydrobiol 123:385–400
Stein LY, Roy R, Dunfield PF (2012) Aerobic Methanotrophy and Nitrification: Processes and Connections. In: Encyclopedia of life sciences (eLS). Wiley, Chichester
Steudler PA, Melillo JM, Feigl BJ, Neill C, Piccolo MC, Cerri CC (1996) Consequence of forest-to-pasture conversion on CH4 fluxes in the Brazilian Amazon Basin. J Geophys Res Atmos 101:18547–18554. https://doi.org/10.1029/96jd01551
Sugimoto A, Wada E (1993) Carbon isotopic composition of bacterial methane in a soil incubation experiment: Contributions of acetate and CO2H2. Geochim Cosmochim Acta 57:4015–4027. https://doi.org/10.1016/0016-7037(93)90350-6
Sugimoto A, Wada E (1995) Hydrogen isotopic composition of bacterial methane: CO2/H2 reduction and acetate fermentation. Geochim Cosmochim Acta 59:1329–1337. https://doi.org/10.1016/0016-7037(95)00047-4
Teh YA, Silver WL, Conrad ME (2005) Oxygen effects on methane production and oxidation in humid tropical forest soils. Glob Chang Biol 11:1283–1297. https://doi.org/10.1111/j.1365-2486.2005.00983.x
Ter Braak CJF, Šmilauer P (2002) Canoco reference manual and canodraw for windows user's guide: Software for canonical community ordination (version 4.5). USA: Microcomputer Power, Ithaca, NY
Torres-Alvarado R, Ramírez-Vives F, Fernández FJ, Barriga-Sosa I (2005) Methanogenesis and methane oxidation in wetlands. Implications in the global carbon cycle. Hidrobiológica 15:327–349
Ueyama M, Yazaki T, Hirano T, Futakuchi Y, Okamura M (2020) Environmental controls on methane fluxes in a cool temperate bog. Agric for Meteorol 281:107852. https://doi.org/10.1016/j.agrformet.2019.107852
United States Environmental Protection Agency – USEPA (2007) Method - Phosphorus determinations in soil samples
Vaksmaa A, Lüke C, Van Alen T, Vale G, Lupotto E, Jetten MS, Ettwig KF (2016) Distribution and activity of the anaerobic methanotrophic community in a nitrogen-fertilized Italian paddy soil. FEMS Microbiol Ecol 92:181. https://doi.org/10.1093/femsec/fiw181
Varner RK, Keller M, Robertson JR, Dias JD, Silva H, Crill PM, McGroddy M, Silver WL (2003) Experimentally induced root mortality increased nitrous oxide emissions from tropical forest soils. Geophys. Res Lett 30:1144. https://doi.org/10.1029/2002GL016164
Wagner D (2017) Effect of varying soil water potentials on methanogenesis in aerated marshland soils. Sci Rep 7:14706. https://doi.org/10.1038/s41598-017-14980-y
Ward N, Larsen Ø, Sakwa J, Bruseth L, Khouri H, Durkin AS et al (2004) Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2:e303. https://doi.org/10.1371/journal.pbio.0020303
Warnes GR et al (2015) Gplots: Various R programming tools for plotting data. R Package Version 2(4):1
Welte CU, Rasigraf O, Vaksmaa A, Versantvoort W, Arshad A, Op den Camp HJ et al (2016) Nitrate- and nitrite-dependent anaerobic oxidation of methane. Environ Microbiol Rep 8:941–955. https://doi.org/10.1111/1758-2229.12487
Whiticar MJ (1999) Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane. Chem Geol 161:291–314. https://doi.org/10.1016/S0009-2541(99)00092-3
Yang Y, Chen J, Tong T, **e S, Liu Y (2020) Influences of eutrophication on methanogenesis pathways and methanogenic microbial community structures in freshwater lakes. Environ Pollut 260:114106. https://doi.org/10.1016/j.envpol.2020.114106
Ye J, Zhang P, Zhang G, Wang S, Nabi M, Zhang Q, Zhang H (2018) Biodesulfurization of high sulfur fat coal with indigenous and exotic microorganisms. J Clean Prod 197:562–570. https://doi.org/10.1016/j.jclepro.2018.06.223
Zhu B, Van Dijk G, Fritz C, Smolders AJ, Pol A, Jetten MS, Ettwig KF (2012) Anaerobic oxidization of methane in a minerotrophic peatland: enrichment of nitrite-ependent methane-oxidizing bacteria. Appl Environ Microbiol 78:8657–8665. https://doi.org/10.1128/AEM.02102-12
Acknowledgements
We wish to thank Dr. Leonardo M. Pitombo, Isadora Leme and Larissa F. Pereira for their excellent technical assistance in lab analysis. We thank Mattias De Hollander, Sainur Samad, Fleur Gawehns, Rodrigo G. Taketani and Tomás Gomes Reis Veloso for bioinformatics support. We also wish to thank João B. Rocha, Ivanildo L. S. Gaia and Domickson Costa for support during field work.
Funding
This study was financed by a Grant from Fundação de Amparo à Pesquisa do Estado do São Paulo – Brasil (FAPESP) (2016/16687-3). MSB was supported by FAPESP 2017/06415-9 and 2018/02277-3. DJB and MGSA were supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Financial Code 001. RR was supported by FAPESP 2017/04665-8. AAN was supported by FAPESP 2017/03575-5. IL was supported by FAPESP 2017/13499-4. LFP was supported by FAPESP 2018/15847-2.
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Bento, M.S., Barros, D.J., Araújo, M.G.S. et al. Active methane processing microbes and the disproportionate role of NC10 phylum in methane mitigation in Amazonian floodplains. Biogeochemistry 156, 293–317 (2021). https://doi.org/10.1007/s10533-021-00846-z
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DOI: https://doi.org/10.1007/s10533-021-00846-z