Skip to main content
Log in

Temporal shift in methanotrophic community and methane oxidation potential in forest soils of dry tropics: high-throughput metagenomic approach

  • Short Communication
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

Forest soil contributes to global methane (CH4) cycle as the natural sink for atmospheric CH4 by methane-oxidizing bacteria (MOB). In this study, high-throughput sequencing of pmoA gene amplicons based approach was used to investigate temporal variations in molecular diversity of MOB in soil of tropical dry forest. Quantitative PCR (qPCR) analysis revealed pmoA and 16S rRNA gene copy numbers (copies g−1 dws) ranging from 2.23 × 106 to 14.62 × 106 and from 0.92 × 109 to 14.99 × 109, respectively, in the year 2016. In 2017, the respective values varied from 1.96 × 106 to 13.62 × 106 and from 2.55 × 109 to 20.15 × 109, respectively. The sequence analysis revealed the existence of both type I and type II methanotrophs in soils. The average observed OTUs were about 800/sample, and Shannon diversity index ranged between 4.24 and 6.22 being highest in winter season. The rice paddy clusters (RPCs), Methylocystis, Methlylocystis-Methylosinus and JR2 and JR3, dominated the methanotrophic community with relative abundance of 32.7–50.2, 15.4–34.2, 0.45–15.8, 0.0–17.8 and 1.6–19.2%, respectively. Relatively, higher CH4 oxidation potential (MOP) (ng CH4 g−1 h−1 dws) was observed in winter (14.12) compared with rainy (2.10) and summer (3.72) coinciding with high methanotrophic diversity and abundance. Overall, the study suggests that tropical dry deciduous forest soils favour considerable range of methanotrophic diversity and abundance that positively correlates with MOP of soils across season.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

References

  • Adamsen APS, King GM (1993) Methane consumption in temperate and subarctic forest soils: rates, vertical zonation, and responses to water and nitrogen. Appl Environ Microbiol 59:485–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amoo AE, Babalola OO (2017) Ammonia-oxidizing microorganisms: key players in the promotion of plant growth. J Soil Sci Plant Nutr 17:935–947

  • Andrew S (2018) A quality control tool for high throughput sequence data. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/

  • Bedard C, Knowles R (1989) Physiology, biochemistry, and specific inhibitors of CH4, NH4+, and CO oxidation by methanotrophs and nitrifiers. Microbiol Rev 53:68–84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bengtson P, Basiliko N, Dumont MG, Hills M, Murrell JC, Roy R, Grayston SJ (2009) Links between methanotroph community composition and CH4 oxidation in a pine forest soil. FEMS Microbiol Ecol 70:356–366

    Article  CAS  PubMed  Google Scholar 

  • Billi D, Potts M (2002) Life and death of dried prokaryotes. Res Microbiol 153:7–12

    Article  CAS  PubMed  Google Scholar 

  • Bodelier PLE, Laanbroek HJ (2004) Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiol Ecol 47:265–277

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña 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, Turnbaugh 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65:5066–5074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng Y, Cui X, Lüke C, Dumont MG (2013) Aerobic methanotroph diversity in Riganqiao peatlands on the Qinghai–Tibetan plateau. Environ Microbiol Rep 5:566–574

    Article  CAS  PubMed  Google Scholar 

  • Dhariwal A, Chong J, Habib S, King IL, Agellon LB, Xia J (2017) MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res 45:W180–W188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dörr N, Glaser B, Kolb S (2010) Methanotrophic communities in Brazilian ferralsols from naturally forested, afforested, and agricultural sites. Appl Environ Microbiol 76:1307–1310

    Article  PubMed  Google Scholar 

  • Dumont MG, Pommerenke B, Fau-Casper P, Casper P (2013) Using stable isotope probing to obtain a targeted metatranscriptome of aerobic methanotrophs in lake sediment. Environ Microbiol Rep 5:757–764

    CAS  PubMed  Google Scholar 

  • Dumont M, Lüke C, Deng Y, Frenzel P (2014) Classification of pmoA amplicon pyrosequences using BLAST and the lowest common ancestor method in MEGAN. Front Microbiol 5:34. https://doi.org/10.3389/fmicb.2014.00034

    Article  PubMed Central  Google Scholar 

  • Dunfield PF (2007) The soil methane sink. In: Reay D, Hewitt CN, Smith K, Grace J (eds) Greenhouse gas sinks, CABI publishing. Wallingford, pp 152–170

  • Dutaur L, Verchot LV (2007) A global inventory of the soil CH4 sink. Global Biogeochem Cycles 21:GB4013. https://doi.org/10.1029/2006GB002734

    Article  CAS  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  • Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative pcr assays. Appl Environ Microbiol 71:4117–4120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geymonat E, Ferrando L, Tarlera SE (2011) Methylogaea oryzae gen. Nov., sp. nov., a mesophilic methanotroph isolated from a rice paddy field. Int J Syst Evol Microbiol 61:2568–2572

    Article  PubMed  Google Scholar 

  • Holmes AJ, Costello A, Lidstrom ME, Murrell JC (1995) Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett 132:203–208

  • Holmes AJ, Roslev P, McDonald IR, Iversen N, Henriksen K, Murrell JC (1999) Characterization of methanotrophic bacterial populations in soils showing atmospheric methane uptake. Appl Environ Microbiol 65:3312–3318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • IBM Corp. Released (2011) IBM SPSS statistics for windows, version 20.0. Armonk, NY: IBM Corp

  • Jaatinen K, Knief C, Dunfield PF, Yrjålå K, Fritze H (2004) Methanotrophic bacteria in boreal forest soil after fire. FEMS Microbiol Ecol 50:195–202

    Article  CAS  PubMed  Google Scholar 

  • Jang I, Lee H, Kang H (2010) The response of nitrogen deposition to methane oxidation availability and microbial enzyme activities in forest soils. Environ Eng Res 15:157–161

    Article  Google Scholar 

  • Judd CR, Koyama A, Simmons MP, Brewer P, von Fischer JC (2016) Co-variation in methanotroph community composition and activity in three temperate grassland soils. Soil Biol Biochem 95:78–86

    Article  CAS  Google Scholar 

  • Kirschke S, Bousquet P, Ciais P, Saunois M, Canadell JG, Dlugokencky EJ, Bergamaschi P, Bergmann D, Blake DR, Bruhwiler L, Cameron-Smith P, Castaldi S, Chevallier F, Feng L, Fraser A, Heimann M, Hodson EL, Houweling S, Josse B, Fraser PJ, Krummel PB, Lamarque J-F, Langenfelds RL, Le Quéré C, Naik V, O'Doherty S, Palmer PI, Pison I, Plummer D, Poulter B, Prinn RG, Rigby M, Ringeval B, Santini M, Schmidt M, Shindell DT, Simpson IJ, Spahni R, Steele LP, Strode SA, Sudo K, Szopa S, van der Werf GR, Voulgarakis A, van Weele M, Weiss RF, Williams JE, Zeng G (2013) Three decades of global methane sources and sinks. Nat Geosci 6:813–823

    Article  CAS  Google Scholar 

  • Knief C (2015) Diversity and habitat preferences of cultivated and uncultivated aerobic methanotrophic bacteria evaluated based on pmoA as molecular marker. Front Microbiol 6:1346. https://doi.org/10.3389/fmicb.2015.01346

    Article  PubMed  PubMed Central  Google Scholar 

  • Knief C, Vanitchung S, Harvey NW, Conrad R, Dunfield PF, Chidthaisong A (2005) Diversity of methanotrophic bacteria in tropical upland soils under different land uses. Appl Environ Microbiol 71:3826–3831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolb S (2009) The quest for atmospheric methane oxidizers in forest soils. Environ Microbiol Rep 1:336–346

    Article  CAS  PubMed  Google Scholar 

  • Kravchenko I, Sukhacheva M (2017) Methane oxidation and diversity of aerobic methanotrophs in forest and agricultural soddy-podzolic soils. Appl Soil Ecol 119:267–274

    Article  Google Scholar 

  • Malghani S, Reim A, von Fischer J, Conrad R, Kuebler K, Trumbore SE (2016) Soil methanotroph abundance and community composition are not influenced by substrate availability in laboratory incubations. Soil Biol Biochem 101:184–194

    Article  CAS  Google Scholar 

  • McDonald IR, Murrell JC (1997) The particulate methane monooxygenase gene pmoA and its use as a functional gene probe for methanotrophs. FEMS Microbiol Lett 156:205–210

    Article  CAS  PubMed  Google Scholar 

  • Nesbit SP, Breitenbeck GA (1992) A laboratory study of factors influencing methane uptake by soils. Agric Ecosyst Environ 41:39–54

    Article  CAS  Google Scholar 

  • Qin H, Tang Y, Shen J, Wang C, Chen C, Yang J, Liu Y, Chen X, Li Y, Hou H (2018) Abundance of transcripts of functional gene reflects the inverse relationship between CH4 and N2O emissions during mid-season drainage in acidic paddy soil. Biol Fertil Soils 54:885–895

    Article  Google Scholar 

  • Saunois M, Bousquet P, Poulter B, Peregon A, Ciais P, Canadell JG, Dlugokencky EJ, Etiope G, Bastviken D, Houweling S, Janssens-Maenhout G, Tubiello FN, Castaldi S, Jackson RB, Alexe M, Arora VK, Beerling DJ, Bergamaschi P, Blake DR, Brailsford G, Brovkin V, Bruhwiler L, Crevoisier C, Crill P, Covey K, Curry C, Frankenberg C, Gedney N, Höglund-Isaksson L, Ishizawa M, Ito A, Joos F, Kim HS, Kleinen T, Krummel P, Lamarque JF, Langenfelds R, Locatelli R, Machida T, Maksyutov S, McDonald KC, Marshall J, Melton JR, Morino I, Naik V, O'Doherty S, Parmentier FJW, Patra PK, Peng C, Peng S, Peters GP, Pison I, Prigent C, Prinn R, Ramonet M, Riley WJ, Saito M, Santini M, Schroeder R, Simpson IJ, Spahni R, Steele P, Takizawa A, Thornton BF, Tian H, Tohjima Y, Viovy N, Voulgarakis A, van Weele M, van der Werf GR, Weiss R, Wiedinmyer C, Wilton DJ, Wiltshire A, Worthy D, Wunch D, Xu X, Yoshida Y, Zhang B, Zhang Z, Zhu Q (2016) The global methane budget 2000–2012. Earth Syst Sci Data 8:697–751

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sengupta A, Dick WA (2017) Methanotrophic bacterial diversity in two diverse soils under varying land-use practices as determined by high-throughput sequencing of the pmoA gene. Appl Soil Ecol 119:35–45

    Article  Google Scholar 

  • Singh BK, Tate K (2007) Biochemical and molecular characterization of methanotrophs in soil from a pristine New Zealand beech forest. FEMS Microbiol Lett 275:89–97

    Article  CAS  PubMed  Google Scholar 

  • Singh JS, Singh S, Raghubanshi AS, Singh S, Kashyap AK, Reddy VS (1997) Effect of soil nitrogen, carbon and moisture on methane uptake by dry tropical forest soils. Plant Soil 196:115–121

    Article  CAS  Google Scholar 

  • Steudler PA, Bowden RD, Melillo JM, Aber JD (1989) Influence of nitrogen fertilization on methane uptake in temperate forest soils. Nature 341:314–316

    Article  Google Scholar 

  • Sultana N, Zhao J, Zheng Y, Cai Y, Faheem M, Peng X, Wang W, Jia Z (2019) Stable isotope probing of active methane oxidizers in rice field soils from cold regions. Biol Fertil Soils 55:243–250

    Article  CAS  Google Scholar 

  • Tsutsumi M, Kojima H, Uemura S, Ono K, Sumida A, Hara T, Fukui M (2009) Structure and activity of soil-inhabiting methanotrophic communities in northern forest of Japan. Soil Biol Biochem 41:403–408

    Article  CAS  Google Scholar 

  • van den Pol-van Dasselaar A, van Beusichem ML, Oenema O (1998) Effects of soil moisture content and temperature on methane uptake by grasslands on sandy soils. Plant Soil 204:213–222

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Vishwakarma P, Dubey SK (2007) The effect of soil type and plant age on the population size of rhizospheric methanotrophs and their activities in tropical rice soils. J Basic Microbiol 47:351–357

    Article  CAS  PubMed  Google Scholar 

  • Vishwakarma P, Singh M, Dubey SK (2010) Changes in methanotrophic community composition after rice crop harvest in tropical soils. Biol Fertil Soils 46:471–479

    Article  Google Scholar 

  • Wei H, Peng C, Liu S, Liu X, Li P, Song H, Yuan M, Wang M (2018) Variation in soil methane fluxes and comparison between two forests in China. Forests 9:1–18. https://doi.org/10.3390/f9040204

    Article  Google Scholar 

  • Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina paired-end reAd mergeR. Bioinformatics 30:614–620

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Adams JM, Dumont MG, Li Y, Shi Y, He D, He J-S, Chu H (2019) Distinct methanotrophic communities exist in habitats with different soil water contents. Soil Biol Biochem 132:143–152

    Article  CAS  Google Scholar 

  • Zhao J-F, Peng S-S, Chen M-P, Wang G-Z, Cui Y-B, Liao L-G, Feng J-G, Zhu B, Liu W-J, Yang L-Y, Tan Z-H (2019) Tropical forest soils serve as substantial and persistent methane sinks. Sci Rep 9:16799. https://doi.org/10.1038/s41598-019-51515-z

Download references

Acknowledgements

We thank the Editor and anonymous reviewers for their critical constructive suggestions on our manuscript.

Funding

This study was financially supported by Department of Science and Technology (DST-SERB), Government of India, New Delhi (File No.: EMR/2014/000502). YB is thankful to CSIR, New Delhi, India (File No: 09/013(0653)/2017-EMR-I), for the financial support in the form of JRF and SRF. We also thank coordinator CAS and DST-FIST for facilities.

Author information

Authors and Affiliations

Authors

Contributions

YB and SKD designed experimentation details. BR helped in sequence analysis. All authors contributed significantly in framing of the manuscript.

Corresponding author

Correspondence to Suresh Kumar Dubey.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest for this publication.

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

(DOC 460 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bhardwaj, Y., Reddy, B. & Dubey, S.K. Temporal shift in methanotrophic community and methane oxidation potential in forest soils of dry tropics: high-throughput metagenomic approach. Biol Fertil Soils 56, 859–867 (2020). https://doi.org/10.1007/s00374-020-01444-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-020-01444-1

Keywords

Navigation