Abstract
Archaea are cosmopolitan in aerated soils around the world. While the dominance of Thaumarchaeota has been reported in most soils, the methanogens are recently found to be ubiquitous but with low abundances in the aerated soil globally. However, the seasonal changes of Archaea community in the aerated soils are still in the mist. In this study, we investigated the change of Archaea in the context of environmental variables over a period of 12 months in a subtropical soil on the Chongming Island, China. The results showed that Nitrososphaera spp. were the dominant archaeal population while the methanogens were in low proportions but highly diverse (including five genera: Methanobacterium, Methanocella, Methanosaeta, Methanosarcina, and Methanomassiliicoccus) in the aerated soil samples determined by high throughput sequencing. A total of 126 LSA correlations were found in the dataset including all the 72 archaeal OTUs and 8 environmental factors. A significance index defined as the pagerank score of each OTU divided by its relative abundance was used to evaluate the significance of each OTU. The results showed that five out of 17 methanogen OTUs were significantly positively correlated with temperature, suggesting those methanogens might increase with temperature rather than being dormant in the aerated soils. Given the metabolic response of methanogens to temperature under aerated soil conditions, their contribution to the global methane cycle warrants evaluation.
Similar content being viewed by others
References
Allen LH, Albrecht SL, Colón-Guasp W, Covell SA, Baker JT, Pan D, Boote KJ (2003) Methane emissions of rice increased by elevated carbon dioxide and temperature. J Environ Qual 32:1978–1991. doi:10.2134/jeq2003.1978
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(4):847–862. doi:10.1038/ismej.2011.141
Angel R, Matthies D, Conrad R (2011) Activation of methanogenesis in arid biological soil crusts despite the presence of oxygen. PLoS One 6(5):e20453. doi:10.1371/journal.pone.0020453
Aschenbach K, Conrad R, Rehakova K, Dolezal J, Janatkova K, Angel R (2013) Methanogens at the top of the world: occurrence and potential activity of methanogens in newly deglaciated soils in high-altitude cold deserts in the Western Himalayas. Front Microbiol 4:359. doi:10.3389/fmicb.2013.00359
Auguet J-C, Barberan A, Casamayor EO (2010) Global ecological patterns in uncultured Archaea. ISME J 4(2):182–190. doi:10.1038/ismej.2009.109
Barberan A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6(2):343–351. doi:10.1038/ismej.2011.119
Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N (2011) Examining the global distribution of dominant archaeal populations in soil. ISME J 5(5):908–917. doi:10.1038/ismej.2010.171
Borrel G, Harris HM, Parisot N, Gaci N, Tottey W, Mihajlovski A, Deane J, Gribaldo S, Bardot O, Peyretaillade E, Peyret P, O'Toole PW, Brugere JF (2013) Genome sequence of “Candidatus Methanomassiliicoccus intestinalis” Issoire-Mx1, a third Thermoplasmatales-related methanogenic archaeon from human feces. Genome Announc 1(4):e00453. doi:10.1128/genomeA.00453-13
Borrel G, Harris HM, Tottey W, Mihajlovski A, Parisot N, Peyretaillade E, Peyret P, Gribaldo S, O'Toole PW, Brugere JF (2012) Genome sequence of “Candidatus Methanomethylophilus alvus” Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogens. J Bacteriol 194(24):6944–6945. doi:10.1128/JB.01867-12
Bouvier T, Del Giorgio P (2007) Key role of selective viral-induced mortality in determining marine bacterial community composition. Environ Microbiol 9(2):287–297
Brioukhanov A, Netrusov A, Sordel M, Thauer RK, Shima S (2000) Protection of Methanosarcina barkeri against oxidative stress: identification and characterization of an iron superoxide dismutase. Arch Microbiol 174(3):213–216. doi:10.1007/s002030000180
Cao P, Zhang LM, Shen JP, Zheng YM, Di HJ, He JZ (2012) Distribution and diversity of archaeal communities in selected Chinese soils. FEMS Microbiol Ecol 80(1):146–158. doi:10.1111/j.1574-6941.2011.01280.x
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336
Cheng W, Chander K, Inubushi K (2000) Effects of elevated CO2 and temperature on methane production and emission from submerged soil microcosm. Nutr Cycl Agroecosyst 58:339–347. doi:10.1007/978-94-010-0898-3_29
Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37(Database issue):D141–D145. doi:10.1093/nar/gkn879
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(7):1844–1853. doi:10.1111/j.1462-2920.2009.01909.x
Cui J, Liu C, Li Z, Wang L, Chen X, Ye Z, Fang C (2012) Long-term changes in topsoil chemical properties under centuries of cultivation after reclamation of coastal wetlands in the Yangtze Estuary, China. Soil Till Res 123:50–60. doi:10.1016/j.still.2012.03.009
DeLong EF (1998) Everything in moderation: Archaea as ‘non-extremophiles’. Curr Opin Genet Dev 8(6):649–654. doi:10.1016/S0959-437X(98)80032-4
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200
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(5785):370–372
Frenzel P, Karofeld E (2000) CH4 emission from a hollow-ridge complex in a raised bog: the role of CH4 production and oxidation. Biogeochemistry 51(1):91–112
Fuhrman JA (2009) Microbial community structure and its functional implications. Nature 459(7244):193–199. doi:10.1038/nature08058
Gantner S, Andersson AF, Alonso-Saez L, Bertilsson S (2011) Novel primers for 16S rRNA-based archaeal community analyses in environmental samples. J Microbiol Meth 84(1):12–18. doi:10.1016/j.mimet.2010.10.001
Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21(3):494–504
He C (1992) Soils of Shanghai. Shanghai Science and Technique Press, Shanghai
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(2):1–11. doi:10.1093/femsec/fiv171
Hu H-W, Zhang L-M, Dai Y, Di H-J, He J-Z (2013a) pH-dependent distribution of soil ammonia oxidizers across a large geographical scale as revealed by high-throughput pyrosequencing. J Soils Sediments 13(8):1439–1449. doi:10.1007/s11368-013-0726-y
Hu H-W, Zhang L-M, Yuan C-L, He J-Z (2013b) Contrasting Euryarchaeota communities between upland and paddy soils exhibited similar pH-impacted biogeographic patterns. Soil Biol Biochem 64:18–27. doi:10.1016/j.soilbio.2013.04.003
Hugoni M, Taib N, Debroas D, Domaizon I, Dufournel IJ, Bronner G, Salter I, Agogué H, Mary I, Galand PE (2013) Structure of the rare archaeal biosphere and seasonal dynamics of active ecotypes in surface coastal waters. Proc Natl Acad Sci U S A 110(15):6004–6009. doi:10.1073/pnas.1216863110
Iino T, Tamaki H, Tamazawa S, Ueno Y, Ohkuma M, Suzuki K-i, Igarashi Y, Haruta S (2013) Candidatus Methanogranum caenicola: a novel methanogen from the anaerobic digested sludge, and proposal of Methanomassiliicoccaceae fam. nov. and Methanomassiliicoccales ord. nov., for a methanogenic lineage of the class Thermoplasmata. Microbes Environ 28(2):244–250. doi:10.1264/jsme2.ME12189
Kitamura K, Fujita T, Akada S, Tonouchi A (2011) Methanobacterium kanagiense sp. nov., a hydrogenotrophic methanogen, isolated from rice-field soil. Int J Syst Evol Microbiol 61(6):1246–1252
Lee CG, Watanabe T, Murase J, Asakawa S, Kimura M (2012) Growth of methanogens in an oxic soil microcosm: elucidation by a DNA-SIP experiment using 13C-labeled dried rice callus. Appl Soil Ecol 58:37–44. doi:10.1016/j.apsoil.2012.03.002
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442(7104):806–809. doi:10.1038/nature04983
Liu CT, Miyaki T, Aono T, Oyaizu H (2008) Evaluation of methanogenic strains and their ability to endure aeration and water stress. Curr Microbiol 56(3):214–218. doi:10.1007/s00284-007-9059-7
Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann N Y Acad Sci 1125(1):171–189. doi:10.1196/annals.1419.019
Lu Y, Conrad R (2005) In situ stable isotope probing of methanogenic archaea in the rice rhizosphere. Science 309:1088–1090. doi:10.1126/science.1113435
Lu Y, Lueders T, Friedrich MW, Conrad R (2005) Detecting active methanogenic populations on rice roots using stable isotope probing. Environ Microbiol 7(3):326–336. doi:10.1111/j.1462-2920.2005.00697.x
Lü Z, Lu Y (2012) Methanocella conradii sp. nov., a thermophilic, obligate hydrogenotrophic methanogen, isolated from Chinese rice field soil. PLoS One 7(4):e35279
Lupatini M, Suleiman AKA, Jacques RJS, Antoniolli ZI, de Siqueira Ferreira AO, Kuramae EE, Roesch LFW (2014) Network topology reveals high connectance levels and few key microbial genera within soils. Front Environ Sci 2:10. doi:10.3389/fenvs.2014.00010
Mayer HP, Conrad R (1990) Factors influencing the population of methanogenic bacteria and the initiation of methane production upon flooding of paddy soil. FEMS Microbiol Ecol 73:103–111. doi:10.1111/j.1574-6968.1990.tb03930.x
Muyzer G, De WEC, Uitterlinden AG (1993) Profiling of complexmicrobial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for16S rRNA. Appl Environ Microbiol 59:695–700
Nicol GW, Glover LA, Prosser JI (2003) Molecular analysis of methanogenic archaeal communities in managed and natural upland pasture soils. Glob Chang Biol 9:1451–1457. doi:10.1046/j.1365-2486.2003.00673.x
Nicol GW, Schleper C (2006) Ammonia-oxidising Crenarchaeota: important players in the nitrogen cycle? Trends Microbiol 14(5):207–212. doi:10.1016/j.tim.2006.03.004
Page L, Brin S, Motwani R, Winograd T (1999) The PageRank citation ranking: bringing order to the web
Paul K, Nonoh JO, Mikulski L, Brune A (2012) “Methanoplasmatales,” Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Appl Environ Microbiol 78(23):8245–8253. doi:10.1128/AEM.02193-12
Pedros-Alio C (2006) Marine microbial diversity: can it be determined? Trends Microbiol 14(6):257–263. doi:10.1016/j.tim.2006.04.007
Pedros-Alio C (2012) The rare bacterial biosphere. Annu Rev Mar Sci 4:449–466. doi:10.1146/annurev-marine-120710-100948
Peng J, Lü Z, Rui J, Lu Y (2008) Dynamics of the methanogenic archaeal community during plant residue decomposition in an anoxic rice field soil. Appl Environ Microbiol 74(9):2894–2901
Peters V, Conrad R (1995) Methanogenic and other strictly anaerobic bacteria in desert soil and other oxic soils. Appl Environ Microbiol 61(4):1673–1676
Poplawski AB, Martensson L, Wartiainen I, Rasmussen U (2007) Archaeal diversity and community structure in a Swedish barley field: specificity of the EK510R/(EURY498) 16S rDNA primer. J Microbiol Methods 69(1):161–173. doi:10.1016/j.mimet.2006.12.018
Praeg N, Wagner AO, Illmer P (2014) Effects of fertilisation, temperature and water content on microbial properties and methane production and methane oxidation in subalpine soils. Eur J Soil Biol 65:96–106. doi:10.1016/j.ejsobi.2014.10.002
Prem EM, Reitschuler C, Illmer P (2014) Livestock grazing on alpine soils causes changes in abiotic and biotic soil properties and thus in abundance and activity of microorganisms engaged in the methane cycle. Eur J Soil Biol 62:22–29. doi:10.1016/j.ejsobi.2014.02.014
Raskin L, Stromley J, Rittmmann B, Stahl D (1994) Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60:1232–1240
Ruan Q, Dutta D, Schwalbach MS, Steele JA, Fuhrman JA, Sun F (2006) Local similarity analysis reveals unique associations among marine bacterioplankton species and environmental factors. Bioinformatics 22(20):2532–2538
Sakai S, Imachi H, Hanada S, Ohashi A, Harada H, Kamagata Y (2008) Methanocella paludicola gen. nov., sp. nov., a methane-producing archaeon, the first isolate of the lineage ‘Rice Cluster I’, and proposal of the new archaeal order Methanocellales ord. nov. Int J Syst Evol Microbiol 58(Pt 4):929–936. doi:10.1099/ijs.0.65571-0
Schleper C, Jurgens G, Jonuscheit M (2005) Genomic studies of uncultivated archaea. Nat Rev Microbiol 3(6):479–488. doi:10.1038/nrmicro1159
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541
Schrope MK, Chanton JP, Allen LH, Baker JT (1999) Effect of CO2 enrichment and elevated temperature on methane emissions from rice Oryza sativa. Glob Chang Biol 5:587–599. doi:10.1111/j.1365-2486.1999.00252.x/full
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504. doi:10.1101/gr.1239303
Shima S, Warkentin E, Grabarse W, Sordel M, Wicke M, Thauer RK, Ermler U (2000) Structure of coenzyme F(420) dependent methylenetetrahydromethanopterin reductase from two methanogenic archaea. J Mol Biol 300(4):935–950. doi:10.1006/jmbi.2000.3909
Sitaula BK, Bakken LR, Abrahamsen G (1995) CH4 uptake by temperate forest soil: effect of N input and soil acidification. Soil Biol Biochem 27(7):871–880. doi:10.1016/0038-0717(95)00017-9
Söllinger A, Schwab C, Weinmaier T, Loy A, Tveit AT, Schleper C, Urich T (2016) Phylogenetic and genomic analysis of Methanomassiliicoccales in wetlands and animal intestinal tracts reveals clade-specific habitat preferences. FEMS Microbiol Ecol 92(1):fiv149
Storey JD (2002) A direct approach to false discovery rates. J Roy Stat Soc B 64(3):479–498. doi:10.1111/1467-9868.00346/full
Takai K, Horikoshi K (1999) Genetic diversity of archaea in deep-sea hydrothermal vent environments. Genetics 152(4):1285–1297
Wang JT, Cao P, Hu HW, Li J, Han LL, Zhang LM, Zheng YM, He JZ (2015) Altitudinal distribution patterns of soil bacterial and archaeal communities along Mt. Shegyla on the Tibetan Plateau. Microb Ecol 69(1):135–145. doi:10.1007/s00248-014-0465-7
Watanabe A, Yamada H, Kimura M (2005) Analysis of temperature effects on seasonal and interannual variation in CH4 emission from rice-planted pots. Agric Ecosyst Environ 105(1–2):439–443. doi:10.1016/j.agee.2004.02.009
Weiss S, Van Treuren W, Lozupone C, Faust K, Friedman J, Deng Y, Xia LC, Xu ZZ, Ursell L, Alm EJ (2016) Correlation detection strategies in microbial data sets vary widely in sensitivity and precision. ISME J
Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A 87(12):4576–4579. doi:10.1073/pnas.87.12.4576
Xie W, Zhang C, Ma C (2015) Temporal variation in community structure and lipid composition of Thaumarchaeota from subtropical soil: insight into proposing a new soil pH proxy. Org Geochem 83:54–64. doi:10.1016/j.orggeochem.2015.02.009
Zhou J, Deng Y, Luo F, He Z, Yang Y (2011) Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. MBio 2(4):e00122–e00111. doi:10.1128/mBio.00122-11
Acknowledgements
We thank Yijie Wang for helping with the field work. This work was supported by The National Science Foundation for Young Scholars of China 41306123 (to WX), National Natural Science Foundation of China 31200986 (to RZ), 41530105 CZ, Natural Science Foundation, the Shanghai Committee of Science and Technology 16ZR1449800 (to RZ) and 13JC1405200 (to CZ), and the Fundamental Research Funds for the Central Universities 1350219165 (to CZ), 10247201546 and 2000219083 (to RZ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
This article does not contain any studies with animals or human participants. All authors confirm that ethical principles have been followed in the experiments as well as in manuscript preparation and approved this submission.
Conflicts of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
ESM 1
(PDF 8146 kb)
Rights and permissions
About this article
Cite this article
Xie, W., Jiao, N., Ma, C. et al. The response of archaeal species to seasonal variables in a subtropical aerated soil: insight into the low abundant methanogens. Appl Microbiol Biotechnol 101, 6505–6515 (2017). https://doi.org/10.1007/s00253-017-8349-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-017-8349-7