Microbial Ecology

, Volume 73, Issue 1, pp 101–110 | Cite as

Salinity Affects the Composition of the Aerobic Methanotroph Community in Alkaline Lake Sediments from the Tibetan Plateau

  • Yongcui Deng
  • Yongqin LiuEmail author
  • Marc Dumont
  • Ralf Conrad
Environmental Microbiology


Lakes are widely distributed on the Tibetan Plateau, which plays an important role in natural methane emission. Aerobic methanotrophs in lake sediments reduce the amount of methane released into the atmosphere. However, no study to date has analyzed the methanotroph community composition and their driving factors in sediments of these high-altitude lakes (>4000 m). To provide new insights on this aspect, the abundance and composition in the sediments of six high-altitude alkaline lakes (including both freshwater and saline lakes) on the Tibetan Plateau were studied. The quantitative PCR, terminal restriction fragment length polymorphism, and 454-pyrosequencing methods were used to target the pmoA genes. The pmoA gene copies ranged 104–106 per gram fresh sediment. Type I methanotrophs predominated in Tibetan lake sediments, with Methylobacter and uncultivated type Ib methanotrophs being dominant in freshwater lakes and Methylomicrobium in saline lakes. Combining the pmoA-pyrosequencing data from Tibetan lakes with other published pmoA-sequencing data from lake sediments of other regions, a significant salinity and alkalinity effect (P = 0.001) was detected, especially salinity, which explained ∼25% of methanotroph community variability. The main effect was Methylomicrobium being dominant (up to 100%) in saline lakes only. In freshwater lakes, however, methanotroph composition was relatively diverse, including Methylobacter, Methylocystis, and uncultured type Ib clusters. This study provides the first methanotroph data for high-altitude lake sediments (>4000 m) and shows that salinity is a driving factor for the community composition of aerobic methanotrophs.


Aerobic methanotrophs High-altitude lake Methylomicrobium Salinity Tibetan Plateau 



We thank Xiaobo Liu for the sample collection, Yanhua Sun for the excellent technical assistance, Andreas Reim for pmoA the database construction, and Pengfei Liu for the data discussion. This work was supported by National Natural Science Foundation of China (Grant No. 41425004 and No. 41401075) and Open Research Fund of Key Laboratory of Tibetan Environmental Changes and Land Surface Processes, CAS (Grant No. TEL201603). Yongcui Deng did the data analyses and first manuscript during her postdoc period in Max Planck Institute for Terrestrial Microbiology. We acknowledge further support by NSF of Jiangsu Province (BK20140923) and PAPD of Jiangsu Higher Education Institutions.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2016_879_MOESM1_ESM.docx (17 kb)
Table S1 (DOCX 16 kb)
248_2016_879_MOESM2_ESM.docx (21 kb)
Table S2 (DOCX 20 kb)
248_2016_879_MOESM3_ESM.docx (27 kb)
Figure S1 (DOCX 26 kb)
248_2016_879_MOESM4_ESM.docx (315 kb)
Figure S2 (DOCX 315 kb)


  1. 1.
    IPCC (2014) In: Core Writing Team, Pachauri RK, Meyer LA (eds) Climate Change 2014: Synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC, Geneva, p 151Google Scholar
  2. 2.
    Bastviken D, Cole J, Pace M et al (2004) Methane emissions from lakes: dependence of lake characteristics, two regional assessments, and a global estimate. Glob Biogeochem Cycles 18:GB4009. doi: 10.1029/2004gb002238 CrossRefGoogle Scholar
  3. 3.
    Frenzel P, Thebrath B, Conrad R (1990) Oxidation of methane in the oxic surface layer of a deep lake sediment (Lake Constance). FEMS Microbiol Ecol 73:149–158. doi: 10.1128/aem.01350-08 CrossRefGoogle Scholar
  4. 4.
    Bowman J (2000) The methanotrophs. The families Methylococcaceae and Methylocystaceae. In: Dworkin M (ed) The prokaryotes. Springer, New York, pp 266–289Google Scholar
  5. 5.
    Semrau JD, DiSpirito AA, Yoon S (2010) Methanotrophs and copper. FEMS Microbiol Rev 34:496–531. doi: 10.1111/j.1574-6976.2010.00212.x CrossRefPubMedGoogle Scholar
  6. 6.
    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. doi: 10.3389/fmicb.2015.01346 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Lüke C, Frenzel P (2011) Potential of pmoA amplicon pyrosequencing for methanotroph diversity studies. Appl Environ Microbiol 77:6305–6309. doi: 10.1128/aem.05355-11 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Dumont MG, Murrell JC (2005) Community-level analysis: key genes of aerobic methane oxidation. Methods Enzymol 397:413–427. doi: 10.1016/s0076-6879(05)97025-0 CrossRefPubMedGoogle Scholar
  9. 9.
    Lin JL, Radajewski S, Eshinimaev BT et al (2004) Molecular diversity of methanotrophs in Transbaikal soda lake sediments and identification of potentially active populations by stable isotope probing. Environ Microbiol 6:1049–1060. doi: 10.1111/j.1462-2920.2004.00635.x CrossRefPubMedGoogle Scholar
  10. 10.
    Rahalkar M, Deutzmann J, Schink B et al (2009) Abundance and activity of methanotrophic bacteria in littoral and profundal sediments of Lake Constance (Germany). Appl Environ Microbiol 75:119–126. doi: 10.1128/aem.01350-08 CrossRefPubMedGoogle Scholar
  11. 11.
    He R, Wooller MJ, Pohlman JW et al (2015) Methane-derived carbon flow through microbial communities in arctic lake sediments. Environ Microbiol 17:3233–3250. doi: 10.1111/1462-2920.12773 CrossRefPubMedGoogle Scholar
  12. 12.
    Yang YY, Zhao Q, Cui YH et al (2015) Spatio-temporal variation of sediment methanotrophic microorganisms in a large eutrophic lake. Microb Ecol 71:9–17. doi: 10.1007/s00248-015-0667-7 CrossRefPubMedGoogle Scholar
  13. 13.
    Liu Y, Zhang JX, Zhao L et al (2015) Aerobic and nitrite-dependent methane-oxidizing microorganisms in sediments of freshwater lakes on the Yunnan Plateau. Appl Microbiol Biotechnol 99:2371–2381. doi: 10.1007/s00253-014-6141-5 CrossRefPubMedGoogle Scholar
  14. 14.
    Khmelenina VN, Eshinimaev BT, Kalyuzhnaya MG et al (2000) Potential activity of methane and ammonium oxidation by methanotrophic communities from the soda lakes of Southern Transbaikal. Microbiology 69:460–465. doi: 10.1007/BF02756771 CrossRefGoogle Scholar
  15. 15.
    Lin JL, Joye SB, Scholten JCM et al (2005) Analysis of methane monooxygenase genes in Mono Lake suggests that increased methane oxidation activity may correlate with a change in methanotroph community structure. Appl Environ Microbiol 71:6458–6462. doi: 10.1128/aem.71.10.6458-6462.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Trotsenko YA, Khmelenina VN (2002) The biology and osmoadaptation of haloalkaliphilie methanotrophs. Microbiology 71:123–132. doi: 10.1023/a:1015183832622 CrossRefGoogle Scholar
  17. 17.
    Khmelenina VN, Kalyuzhnaya MG, Starostina NG et al (1997) Isolation and characterization of halotolerant alkaliphilic methanotrophic bacteria from Tuva soda lakes. Curr Microbiol 35:257–261. doi: 10.1007/s002849900249 CrossRefGoogle Scholar
  18. 18.
    Sorokin DY, Kuenen JG (2005) Chemolithotrophic haloalkaliphiles from soda lakes. FEMS Microbiol Ecol 52:287–295. doi: 10.1016/j.femsec.2005.02.012 CrossRefPubMedGoogle Scholar
  19. 19.
    Eshinimaev BT, Khmelenina VN, Trotsenko YA (2008) First isolation of a type II methanotroph from a soda lake. Microbiology 77:628–631. doi: 10.1134/s0026261708050196 CrossRefGoogle Scholar
  20. 20.
    Carini S, Bano N, LeCleir G et al (2005) Aerobic methane oxidation and methanotroph community composition during seasonal stratification in Mono Lake, California (USA). Environ Microbiol 7:1127–1138. doi: 10.1111/j.1462-2920.2005.00786.x CrossRefPubMedGoogle Scholar
  21. 21.
    Bian D, Yang Z, Li L et al (2006) The response of lake area change to climate variations in north Tibetan Plateau during last 30 years. Acta Geol Sin 5:510–518Google Scholar
  22. 22.
    Zheng M (1997) An introduction to saline lakes on the Qinghai-Tibet Plateau. Springer, NetherlandsGoogle Scholar
  23. 23.
    He R, Wooller MJ, Pohlman JW et al (2012) Identification of functionally active aerobic methanotrophs in sediments from an arctic lake using stable isotope probing. Environ Microbiol 14:1403–1419. doi: 10.1111/j.1462-2920.2012.02725.x CrossRefPubMedGoogle Scholar
  24. 24.
    Xiong JB, Liu YQ, Lin XG et al (2012) Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ Microbiol 14:2457–2466. doi: 10.1111/j.1462-2920.2012.02799.x CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Liu YQ, Yao TD, Jiao NZ et al (2013) Salinity impact on bacterial community composition in five high-altitude lakes from the Tibetan Plateau, Western China. Geomicrobiol J 30:462–469. doi: 10.1080/01490451.2012.710709 CrossRefGoogle Scholar
  26. 26.
    Liu YQ, Priscu JC, Xiong JB et al (2016) Salinity drives archaeal distribution patterns in high altitude lake sediments on the Tibetan Plateau. FEMS Microbiol Ecol. doi: 10.1093/femsec/fiw033 Google Scholar
  27. 27.
    Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65:5066–5074PubMedPubMedCentralGoogle Scholar
  28. 28.
    Kolb S, Knief C, Stubner S et al (2003) Quantitative detection of methanotrophs in soil by novel pmoA-targeted real-time PCR assays. Appl Environ Microbiol 69:2423–2429. doi: 10.1128/aem.69.5.2423-2429.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Deng YC, Cui XY, Lüke C et al (2013) Aerobic methanotroph diversity in Riganqiao peatlands on the Qinghai-Tibetan Plateau. Environ Microbiol Rep 5:566–574. doi: 10.1111/1758-2229.12046 CrossRefPubMedGoogle Scholar
  30. 30.
    Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi: 10.1128/aem.01541-09 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Dumont MG, Pommerenke B, Casper P et al (2011) DNA-, rRNA- and mRNA-based stable isotope probing of aerobic methanotrophs in lake sediment. Environ Microbiol 13:1153–1167. doi: 10.1111/j.1462-2920.2010.02415.x CrossRefPubMedGoogle Scholar
  32. 32.
    Kim OS (2007) Diversity of functional genes in the aquatic nitrogen cycle. PhD Thesis, Christian-Albrechts-Universität, KielGoogle Scholar
  33. 33.
    Antony CP, Kumaresan D, Hunger S et al (2013) Microbiology of Lonar Lake and other soda lakes. ISME J 7:468–476. doi: 10.1038/ismej.2012.137 CrossRefPubMedGoogle Scholar
  34. 34.
    Ludwig W, Strunk O, Westram R et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371. doi: 10.1093/nar/gkh293 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    De Mendiburu F, Simon R (2015) Agricolae—ten years of an open source statistical tool for experiments in breeding, agriculture and biology. PeerJ PrePrints 3, e1748. doi: 10.7287/peerj.preprints.1404v1 Google Scholar
  36. 36.
    Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525. doi: 10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2 CrossRefGoogle Scholar
  37. 37.
    Hammer UT (1986) Saline lake ecosystems of the world. Dr W Junk, DordrechtGoogle Scholar
  38. 38.
    Oksanen J, Blanchet FG, Kindt R et al (2016) Vegan: community ecology packageGoogle Scholar
  39. 39.
    Wang SM, Dou HS (1998) Chinese lake records. Science Press, BeijingGoogle Scholar
  40. 40.
    Schlegel I, Scheffler W (1999) Seasonal development and morphological variability of Cyclotella ocellata (Bacillariophyceae) in the eutrophic Lake Dagow (Germany). Int Rev Hydrobiol 84:469–478. doi: 10.1002/iroh.199900041 Google Scholar
  41. 41.
    Salka I, Cuperova Z, Masin M et al (2011) Rhodoferax-related pufM gene cluster dominates the aerobic anoxygenic phototrophic communities in German freshwater lakes. Environ Microbiol 13:2865–2875. doi: 10.1111/j.1462-2920.2011.02562.x CrossRefPubMedGoogle Scholar
  42. 42.
    Furtado ALS, Casper P, Esteves FA (2001) Bacterioplankton abundance, biomass and production in a Brazilian coastal lagoon and in two German lakes. An Acad Bras Cienc 73:39–49. doi: 10.1590/s0001-37652001000100005 CrossRefPubMedGoogle Scholar
  43. 43.
    Krambeck HJ, Albrecht D, Hickel B, Hofmann W, Arzbach HH (1993) Limnology of the Plußsee. In: Overbeck J, Chrost RJ (eds) Microbial ecology of Lake Plußsee. Springer, New York, pp 1–23Google Scholar
  44. 44.
    Liu XL, Hou WG, Dong HL et al (2015) Distribution and diversity of Cyanobacteria and eukaryotic algae in Qinghai-Tibetan lakes. Geomicrobiol J. doi: 10.1080/01490451.2015.1120368 Google Scholar
  45. 45.
    Yang J, Ma LA, Jiang HC et al (2016) Salinity shapes microbial diversity and community structure in surface sediments of the Qinghai-Tibetan lakes. Sci Rep 6:25078. doi: 10.1038/srep25078 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Kaluzhnaya M, Khmelenina V, Eshinimaev B et al (2001) Taxonomic characterization of new alkaliphilic and alkalitolerant methanotrophs from soda lakes of the Southeastern Transbaikal region and description of Methylomicrobium buryatense sp.nov. Syst Appl Microbiol 24:166–176. doi: 10.1078/0723-2020-00028 CrossRefPubMedGoogle Scholar
  47. 47.
    Kalyuzhnaya MG, Khmelenina V, Eshinimaev B et al (2008) Classification of halo(alkali)philic and halo(alkali)tolerant methanotrophs provisionally assigned to the genera Methylomicrobium and Methylobacter and emended description of the genus Methylomicrobium. Int J Syst Evol Micrbiol 58:591–596. doi: 10.1099/ijs.0.65317-0 CrossRefGoogle Scholar
  48. 48.
    Khmelenina VN, Shchukin VN, Reshetnikov AS et al (2010) Structural and functional features of methanotrophs from hypersaline and alkaline lakes. Microbiology 79:472–482. doi: 10.1134/s0026261710040090 CrossRefGoogle Scholar
  49. 49.
    Sorokin DY, Gorlenko VM, Namsaraev BB et al (2004) Prokaryotic communities of the north-eastern Mongolian soda lakes. Hydrobiologia 522:235–248. doi: 10.1023/B:HYDR.0000029989.73279.e4 CrossRefGoogle Scholar
  50. 50.
    Antony CP, Kumaresan D, Ferrando L et al (2010) Active methylotrophs in the sediments of Lonar Lake, a saline and alkaline ecosystem formed by meteor impact. ISME J 4:1470–1480. doi: 10.1038/ismej.2010.70 CrossRefPubMedGoogle Scholar
  51. 51.
    Deutzmann JS, Woerner S, Schink B (2011) Activity and diversity of methanotrophic bacteria at methane seeps in eastern Lake Constance sediments. Appl Environ Microbiol 77:2573–2581. doi: 10.1128/aem.02776-10 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Siljanen HMP, Saari A, Krause S et al (2011) Hydrology is reflected in the functioning and community composition of methanotrophs in the littoral wetland of a boreal lake. FEMS Microbiol Ecol 75:430–445. doi: 10.1111/j.1574-6941.2010.01015.x CrossRefPubMedGoogle Scholar
  53. 53.
    Yun JL, Ma AZ, Li YM et al (2010) Diversity of methanotrophs in Zoige wetland soils under both anaerobic and aerobic conditions. J Environ Sci 22:1232–1238. doi: 10.1016/s1001-0742(09)60243-6 CrossRefGoogle Scholar
  54. 54.
    Yun JL, Zhuang GQ, Ma AZ et al (2012) Community structure, abundance, and activity of methanotrophs in the Zoige wetland of the Tibetan Plateau. Microbial Ecol 63:835–843. doi: 10.1007/s00248-011-9981-x CrossRefGoogle Scholar
  55. 55.
    Chen Y, Dumont MG, Cebron A et al (2007) Identification of active methanotrophs in a landfill cover soil through detection of expression of 16S rRNA and functional genes. Environ Microbiol 9:2855–2869. doi: 10.1111/j.1462-2920.2007.01401.x CrossRefPubMedGoogle Scholar
  56. 56.
    Chen Y, Dumont MG, McNamara NP et al (2008) Diversity of the active methanotrophic community in acidic peatlands as assessed by mRNA and SIP-PLFA analyses. Environ Microbiol 10:446–459. doi: 10.1111/j.1462-2920.2007.01466.x CrossRefPubMedGoogle Scholar
  57. 57.
    Kip N, van Winden JF, Pan Y et al (2010) Global prevalence of methane oxidation by symbiotic bacteria in peat-moss ecosystems. Nat Geosci 3:617–621. doi: 10.1038/ngeo939 CrossRefGoogle Scholar
  58. 58.
    Dedysh SN (2009) Exploring methanotroph diversity in acidic northern wetlands: molecular and cultivation-based studies. Microbiology 78:655–669. doi: 10.1134/S0026261709060010 CrossRefGoogle Scholar
  59. 59.
    Horz HP, Yimga MT, Liesack W (2001) Detection of methanotroph diversity on roots of submerged rice plants by molecular retrieval of pmoA, mmoX, mxaF, and 16S rRNA and ribosomal DNA, including pmoA-based terminal restriction fragment length polymorphism profiling. Appl Environ Microbiol 67:4177–4185. doi: 10.1128/AEM.67.9.4177-4185.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Reim A, Lüke C, Krause S et al (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. doi: 10.1038/ismej.2012.57 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Yongcui Deng
    • 1
    • 2
    • 3
  • Yongqin Liu
    • 4
    Email author
  • Marc Dumont
    • 5
  • Ralf Conrad
    • 2
  1. 1.College of Geographic SciencesNanjing Normal UniversityNanjingChina
  2. 2.Max Planck Institute for Terrestrial MicrobiologyMarburgGermany
  3. 3.Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and ApplicationNanjingChina
  4. 4.Key Laboratory of Tibetan Environment Changes and Land Surface Processes, Institute of Tibetan Plateau ResearchChinese Academy of SciencesBeijingChina
  5. 5.Biological SciencesUniversity of SouthamptonSouthamptonUK

Personalised recommendations