Abstract
DNA-based stable isotope probing (DNA-SIP) was employed to establish direct link between methane oxidation activity and the taxonomic identity of active methanotrophs in three rice field soils from Jian-San-Jiang (one baijiang origin soil, JB and one meadow origin soil, JM) and Qing-An (meadow origin soil, QA) districts in Northeastern China. Following microcosm incubation under 1% v/v13CH4 condition, soil organic 13C atom percent significantly increased from background 1.08 to 1.21% in average, indicating the biomass synthesis supported by methanotrophy. Real-time PCR analysis of methanotroph-specific biomarker pmoA genes of the buoyant density for DNA gradient, following the ultracentrifugation of the total DNA extracted from SIP microcosms, indicated an enrichment of methanotroph genomes in 13C-labeled DNA. It suggested propagation of microbial methane oxidizers in soils. High-throughput sequencing of 16S rRNA and pmoA genes from 13C-labeled DNA further revealed a diverse guild of both type I and II methanotrophs in all three soils. Specifically, Methylobacter-affiliated type I methanotrophs dominated the methanotrophic activity in JB and JM soils, whereas Methylocystis-affiliated type II methanotrophs dominated QA soil. This implied the physiological diversification of soil methanotrophs that might be due to constant environmental fluctuations in paddies.
References
Bodelier PLE, Laanbroek HJ (2004) Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiol Ecol 47:265–277
Bodelier P, Roslev P, Henckel T, Frenzel P (2000) Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots. Nature 403:421–424
Cai Y, Zheng Y, Bodelier PL, Conrad R, Jia Z (2016) Conventional methanotrophs are responsible for atmospheric methane oxidation in paddy soils. Nat Commun 7:11728
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Chen Y, Dumont MG, McNamara NP, Chamberlain PM, Bodrossy L, Stralis-Pavese N, Murrell JC (2008a) Diversity of the active methanotrophic community in acidic peatlands as assessed by mRNA and SIP-PLFA analyses. Environ Microbiol 10:446–459
Chen Y, Dumont MG, Neufeld JD, Bodrossy L, Stralis-Pavese N, McNamara NP, Ostle N, Briones MJ, Murrell JC (2008b) Revealing the uncultivated majority: combining DNA stable-isotope probing, multiple displacement amplification and metagenomic analyses of uncultivated Methylocystis in acidic peatlands. Environ Microbiol 10:2609–2622
Conrad R, Rothfuss F (1991) Methane oxidation in the soil surface layer of a flooded rice field and the effect of ammonium. Biol Fertil Soils 12:28–32
Dedysh SN (2009) Exploring methanotroph diversity in acidic northern wetlands: molecular and cultivation-based studies. Microbiology 78:655–669
Eller G, Frenzel P (2001) Changes in activity and community structure of methane-oxidizing bacteria over the growth period of rice. Appl Environ Microbiol 67:2395–2403
Esson KC, Lin X, Kumaresan D, Chanton JP, Murrell JC, Kostka JE (2016) Alpha- and gammaproteobacterial methanotrophs codominate the active methane-oxidizing communities in an acidic boreal peat bog. Appl Environ Microbiol 82:2363–2371
Frenzel P, Rothfuss F, Conrad R (1992) Oxygen profiles and methane turnover in a flooded rice microcosm. Biol Fertil Soils 14:84–89
Graef C, Hestnes AG, Svenning MM, Frenzel P (2011) The active methanotrophic community in a wetland from the high Arctic. Environ Microbiol Rep 3:466–472
Gupta V, Smemo KA, Yavitt JB, Basiliko N (2012) Active methanotrophs in two contrasting north American peatland ecosystems revealed using DNA-SIP. Microb Ecol 63:438–445
Hahn J, Juottonen H, Fritze H, Tuittila E-S (2018) Dung application increases CH4 production potential and alters the composition and abundance of methanogen community in restored peatland soils from Europe. Biol Fertil Soils 54:533–547
Hanson R, Hanson T (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471
He R, Wooller MJ, Pohlman JW, Quensen J, Tiedje JM, Leigh MB (2012) Diversity of active aerobic methanotrophs along depth profiles of arctic and subarctic lake water column and sediments. ISME J 6:1937–1948
Ho A, Kerckhof FM, Luke C, Reim A, Krause S, Boon N, Bodelier PL (2013) Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies. Environ Microbiol Rep 5:335–345
Huang S, Sun Y, Yu X, Zhang W (2015) Interactive effects of temperature and moisture on CO2 and CH4 production in a paddy soil under long-term different fertilization regimes. Biol Fertil Soils 52:285–294
IPCC (2013) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change (eds Stocker TF et al). Cambridge University Press, Cambridge
Jia Z, Conrad R (2009) Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671
Kip N, Fritz C, Langelaan ES, Pan Y, Bodrossy L, Pancotto V, Jetten MSM, Smolders AJP, Op den Camp HJM (2012) Methanotrophic activity and diversity in different Sphagnum magellanicum dominated habitats in the southernmost peat bogs of Patagonia. Biogeosciences 9:47–55
Knief C, Dunfield PF (2005) Response and adaptation of different methanotrophic bacteria to low methane mixing ratios. Environ Microbiol 7:1307–1317
Luke C, Frenzel FP, Ho A, Fiantis D, Schad P, Schneider B, Schwark L, Utami SR (2014) Macroecology of methane-oxidizing bacteria: the β-diversity of pmoA genotypes in tropical and subtropical rice paddies. Environ Microbiol 16:72–83
Ma K, Conrad R, Lu Y (2013) Dry/wet cycles change the activity and population dynamics of methanotrophs in rice field soil. Appl Environ Microbiol 79:4932–4939
Macalady J, McMillan A, Dickens A, Tyler S, Scow K (2002) Population dynamics of type I and II methanotrophic bacteria in rice soils. Environ Microbiol 4:148–157
Mayumi D, Yoshimoto T, Uchiyama H, Nomura N, Nakajima-Kambe T (2010) Seasonal change in methanotrophic diversity and populations in a rice field soil assessed by DNA-stable isotope probing and quantitative real-time PCR. Microbes Environ 25:156–163
Mohanty SR, Bodelier PL, Floris V, Conrad R (2006) Differential effects of nitrogenous fertilizers on methane-consuming microbes in rice field and forest soils. Appl Environ Microbiol 72:1346–1354
Noll M, Frenzel P, Conrad R (2008) Selective stimulation of type I methanotrophs in a rice paddy soil by urea fertilization revealed by RNA-based stable isotope probing. FEMS Microbiol Ecol 65:125–132
Nouchi I, Mariko S, Aoki K (1990) Mechanism of methane transport from the rhizosphere to the atmosphere through rice plants. Plant Physiol 94:59–66
Nouchi I, Hosono T, Aoki K, Minami K (1994) Seasonal-variation in methane flux from rice paddies associated with methane concentration in soil-water, rice biomass and temperature and its modeling. Plant Soil 161:195–208
Qiu Q, Noll M, Abraham WR, Lu Y, Conrad R (2008) Applying stable isotope probing of phospholipid fatty acids and rRNA in a Chinese rice field to study activity and composition of the methanotrophic bacterial communities in situ. ISME J 2:602–614
Reim A, Luke C, Krause S, Pratscher J, Frenzel P (2012) One millimetre makes the difference: high-resolution analysis of methane-oxidizing bacteria and their specific activity at the oxic-anoxic interface in a flooded paddy soil. ISME J 6:2128–2139
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Schöler A, Jacquiod S, Vestergaard G, Schulz S, Schloter M (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Fertil Soils 53:485–489
Shiau YJ, Cai Y, Jia Z, Chen CL, Chiu CY (2018) Phylogenetically distinct methanotrophs modulate methane oxidation in rice paddies across Taiwan. Soil Biol Biochem 124:59–69
Shrestha M, Abraham WR, Shrestha PM, Noll M, Conrad R (2008) Activity and composition of methanotrophic bacterial communities in planted rice soil studied by flux measurements, analyses of pmoA gene and stable isotope probing of phospholipid fatty acids. Environ Microbiol 10:400–412
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 40. Mol Biol Evol 24:1596–1599
Tang S, Cheng W, Hu R, Guigue J, Kimani SM, Tawaraya K, Xu X (2016) Simulating the effects of soil temperature and moisture in the off-rice season on rice straw decomposition and subsequent CH4 production during the growth season in a paddy soil. Biol Fertil Soils 52:739–748
Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart-how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484
Walkiewicz A, Brzezińska M, Bieganowski A (2018) Methanotrophs are favored under hypoxia in ammonium-fertilized soils. Biol Fertil Soils 54:861–870
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
Wang B, Zhao J, Guo Z, Ma J, Xu H, Jia Z (2015) Differential contributions of ammonia oxidizers and nitrite oxidizers to nitrification in four paddy soils. ISME J 9:1062–1075
Wartiainen I, Hestnes AG, McDonald IR, Svenning MM (2006) Methylocystis rosea sp. nov., a novel methanotrophic bacterium from Arctic wetland soil, Svalbard, Norway (78 degrees N). Int J Syst Evol Microbiol 56:541–547
Xia WW, Zhang CX, Zeng XW, Feng YZ, Weng JH, Lin XG, Zhu JG, Xiong ZQ, Xu J, Cai ZC, Jia ZJ (2011) Autotrophic growth of nitrifying community in an agricultural soil. ISME J 5:1226–1236
Zhang X, Yin S, Li Y, Zhuang H, Li C, Liu C (2014) Comparison of greenhouse gas emissions from rice paddy fields under different nitrogen fertilization loads in Chongming Island. Eastern China Sci Total Environ 472:381–388
Zhao J, Wang B, Jia Z (2015) Phylogenetically distinct phylotypes modulate nitrification in a paddy soil. Appl Environ Microbiol 81:3218–3227
Zheng Y, Zhang LM, Zheng YM, Di H, He JZ (2008) Abundance and community composition of methanotrophs in a Chinese paddy soil under long-term fertilization practices. J Soils Sediments 8:406–414
Zheng Y, Huang R, Wang BZ, Bodelier PLE, Jia ZJ (2014) Competitive interactions between methane- and ammonia-oxidizing bacteria modulate carbon and nitrogen cycling in paddy soil. Biogeosciences 11:3353–3368
Acknowledgments
Nasrin Sultana gratefully acknowledged the Organization for Women in Science for the Developing World (OWSD) for a PhD Fellowship program.
Funding
This study is financially supported by the National Science Foundation of P.R. China (41501276, 41701302, 91751204), the Open Foundation of the Heilongjiang Provincial Key Laboratory of Environmental Microbiology and Recycling of Argo-Waste in Cold Region (201714), and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15040000).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 1239 kb)
Rights and permissions
About this article
Cite this article
Sultana, N., Zhao, J., Zheng, Y. et al. Stable isotope probing of active methane oxidizers in rice field soils from cold regions. Biol Fertil Soils 55, 243–250 (2019). https://doi.org/10.1007/s00374-018-01334-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-018-01334-7