Advertisement

Journal of Earth Science

, Volume 30, Issue 2, pp 387–396 | Cite as

Bacterial Diversity in Alpine Lakes: A Review from the Third Pole Region

  • Namita Paudel AdhikariEmail author
  • Subash Adhikari
  • Xiaobo LiuEmail author
  • Liang Shen
  • Zhengquan Gu
Biogeology and Marine Geology
  • 15 Downloads

Abstract

Microorganisms are unique among all of the living organisms because of their high population size, advanced genetic diversity, short generation time, and quick response to the small change in environmental conditions. Remote alpine lakes of the Third Pole region provide the unique habitat for microorganisms acting as a natural laboratory and offering the information about the ecological roles of microorganisms. Many researchers focused on microbial communities as well as the impact of physicochemical, biological and hydrological parameters in lakes of this region since decades but the comprehensive review focusing on bacterial diversity and the role of environmental parameters still lacks. Here we reviewed bacterial diversity in lakes of the Third Pole region by analyzing 16S rRNA clone libraries accessed from previous research findings. A total of 5 388 bacterial 16S rRNA gene sequences were analyzed and classified into different phylogenetic groups. The average relative abundance of dominant taxa includes Betaproteobacteria (19%), Bacteroidetes (18%), Gammaproteobacteria (16%), Actinobacteria (15%), Alphaproteobacteria (14%), Cyanobacteria (7%), and Firmicutes (5%). Several adaptational strategies were adopted by these dominant bacterial groups in order to accommodate in the respective habitat. Nevertheless, lake water properties like temperature, pH, salinity, incident UV radiation, turbidity, and nutrients also played role in bacterial diversity.

Key Words

bacterial diversity alpine lakes 16S rRNA Third Pole region 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (No. 41425004). The final publication is available at Springer via  https://doi.org/10.1007/s12583-018-1206-5.

References Cited

  1. Arifuzzaman, M., Khatun, M. R., Rahman, H., 2010. Isolation and Screening of Actinomycetes from Sundarbans Soil for Antibacterial Activity. African Journal of Biotechnology, 9(29): 4615–4619Google Scholar
  2. Berg, K. A., Lyra, C., Sivonen, K., et al., 2008. High Diversity of Cultivable Heterotrophic Bacteria in Association with Cyanobacterial Water Blooms. The ISME Journal, 3(3): 314–325.  https://doi.org/10.1038/ismej.2008.110 Google Scholar
  3. Bergström, A. K., 2010. The Use of TN: TP and DIN: TP Ratios as Indicators for Phytoplankton Nutrient Limitation in Oligotrophic Lakes Affected by N Deposition. Aquatic Sciences, 72(3): 277–281.  https://doi.org/10.1007/s00027-010-0132-0 Google Scholar
  4. Brahney, J., Mahowald, N., Ward, D. S., et al., 2015. Is Atmospheric Phosphorus Pollution Altering Global Alpine Lake Stoichiometry?. Global Biogeochemical Cycles, 29(9): 1369–1383.  https://doi.org/10.1002/2015gb005137 Google Scholar
  5. Cao, X. F., Wang, J., Liao, J. Q., et al., 2017. Bacterioplankton Community Responses to Key Environmental Variables in Plateau Freshwater Lake Ecosystems: A Structural Equation Modeling and Change Point Analysis. Science of the Total Environment, 580(5): 457–467.  https://doi.org/10.1016/j.scitotenv.2016.11.143 Google Scholar
  6. Casamayor, E. O., Schafer, H., Baneras, L., et al., 2000. Identification of and Spatio-Temporal Differences between Microbial Assemblages from Two Neighboring Sulfurous Lakes: Comparison by Microscopy and Denaturing Gradient Gel Electrophoresis. Applied and Environmental Microbiology, 66(2): 499–508.  https://doi.org/10.1128/aem.66.2.499-508.2000 Google Scholar
  7. Catherine, Q., Susanna, W., Isidora, E. S., et al., 2013. A Review of Current Knowledge on Toxic Benthic Freshwater Cyanobacteria—Ecology, Toxin Production and Risk Management. Water Research, 47(15): 5464–5479.  https://doi.org/10.1016/j.watres.2013.06.042 Google Scholar
  8. Cole, J. J., Prairie, Y. T., Caraco, N. F., et al., 2007. Plumbing the Global Carbon Cycle: Integrating Inland Waters into the Terrestrial Carbon Budget. Ecosystems, 10(1): 172–185.  https://doi.org/10.1007/s10021-006-9013-8 Google Scholar
  9. Dai, Y., Yang, Y. Y., Wu, Z., et al., 2016. Spatiotemporal Variation of Planktonic and Sediment Bacterial Assemblages in Two Plateau Freshwater Lakes at Different Trophic Status. Applied Microbiology and Biotechnology, 100(9): 4161–4175.  https://doi.org/10.1007/s00253-015-7253-2 Google Scholar
  10. Diego, F., Yamila, B., Gisela, M., et al., 2015. Controlling Factors in Planktonic Communities over a Salinity Gradient in High-Altitude Lakes. Annales de Limnologie-International Journal of Limnology, 51(3): 261–272.  https://doi.org/10.1051/limn/2015020 Google Scholar
  11. Dong, H. L., Jiang, H. C., Yu, B. S., et al., 2010. Impacts of Environmental Change and Human Activity on Microbial Ecosystems on the Tibetan Plateau, NW China. GSA Today, 20(6): 4–10.  https://doi.org/10.1130/gsatg75a.1 Google Scholar
  12. Downing, J. A., Prairie, Y. T., Cole, J. J., et al., 2006. The Global Abundance and Size Distribution of Lakes, Ponds, and Impoundments. Limnology and Oceanography, 51(5): 2388–2397.  https://doi.org/10.4319/lo.2006.51.5.2388 Google Scholar
  13. Dunbar, J., Takala, S., Barns, S. M., et al., 1999. Levels of Bacterial Community Diversity in Four Arid Soils Compared by Cultivation and 16S rRNA Gene Cloning. Applied and Environmental Microbiology, 65(4): 1662–1669Google Scholar
  14. Eiler, A., Langenheder, S., Bertilsson, S., et al., 2003. Heterotrophic Bacterial Growth Efficiency and Community Structure at Different Natural Organic Carbon Concentrations. Applied and Environmental Microbiology, 69(7): 3701–3709.  https://doi.org/10.1128/aem.69.7.3701-3709.2003 Google Scholar
  15. Guan, X. Y., Wang, J. F., Zhao, H., et al., 2013. Soil Bacterial Communities Shaped by Geochemical Factors and Land Use in a Less-Explored Area, Tibetan Plateau. BMC Genomics, 14(1): 820.  https://doi.org/10.1186/1471-2164-14-820 Google Scholar
  16. Hengstmann, U. L. F., Chin, K., Janssen, P. H., et al., 1999. Comparative Phylogenetic Assignment of Environmental Sequences of Genes Encoding 16S rRNA and Numerically Abundant Culturable Bacteria from an Anoxic Rice Paddy Soil. Applied and Environmental Microbiology, 65(11): 5050–5058Google Scholar
  17. Hood, E., Fellman, J., Spencer, R. G. M., et al., 2009. Glaciers as a Source of Ancient and Labile Organic Matter to the Marine Environment. Nature, 462(7276): 1044–1047.  https://doi.org/10.1038/nature08580 Google Scholar
  18. Hu, A. Y., Yao, T. D., Jiao, N. Z., et al., 2010. Community Structures of Ammonia-Oxidising Archaea and Bacteria in High-Altitude Lakes on the Tibetan Plateau. Freshwater Biology, 55(11): 2375–2390.  https://doi.org/10.1111/j.1365-2427.2010.02454.x Google Scholar
  19. Jezbera, J., Jezberová, J., Koll, U., et al., 2012. Contrasting Trends in Distribution of Four Major Planktonic Betaproteobacterial Groups along a PH Gradient of Epilimnia of 72 Freshwater Habitats. FEMS Microbiology Ecology, 81(2): 467–479.  https://doi.org/10.1111/j.1574-6941.2012.01372.x Google Scholar
  20. Jiang, H., Dong, H., Zhang, G., et al., 2006. Microbial Diversity in Water and Sediment of Lake Chaka, an Athalassohaline Lake in Northwestern China. Applied and Environmental Microbiology, 72(6): 3832–3845.  https://doi.org/10.1128/aem.02869-05 Google Scholar
  21. Karentz, D., Bothwell, M. L., Coffin, R. B., et al., 1994. Impact of UV-B Radiation on Pelagic Freshwater Ecosystems: Report of Working Group on Bacteria and Phytoplankton. Advances in Limnology, 43(9): 31–69Google Scholar
  22. Kirchman, D. L., Dittel, A. I., Findlay, S. E. G., et al., 2004. Changes in Bacterial Activity and Community Structure in Response to Dissolved Organic Matter in the Hudson River, New York. Aquatic Microbial Ecology, 35: 243–257.  https://doi.org/10.3354/ame035243 Google Scholar
  23. Klug, J. L., Fischer, J. M., Ives, A. R., et al., 2000. Compensatory Dynamics in Planktonic Community Responses to pH Perturbations. Ecology, 81(2): 387–398.  https://doi.org/10.1890/0012-9658(2000)081[0387:cdipcr]2.0.co;2 Google Scholar
  24. Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33(7): 1870–1874.  https://doi.org/10.1093/molbev/msw054 Google Scholar
  25. Lindström, E. S., Kamst-Van Agterveld, M. P., Zwart, G., 2005. Distribution of Typical Freshwater Bacterial Groups is Associated with pH, Temperature, and Lake Water Retention Time. Applied and Environmental Microbiology, 71(12): 8201–8206.  https://doi.org/10.1128/aem.71.12.8201-8206.2005 Google Scholar
  26. Liu, K. S., Liu, Y. Q., Jiao, N. Z., et al., 2016. Vertical Variation of Bacterial Community in Nam Co, a Large Stratified Lake in Central Tibetan Plateau. Antonie van Leeuwenhoek, 109(10): 1323–1335.  https://doi.org/10.1007/s10482-016-0731-4 Google Scholar
  27. Liu, K. S., Liu, Y. Q., Jiao, N. Z., et al., 2017. Bacterial Community Composition and Diversity in Kalakuli, an Alpine Glacial-Fed Lake in Muztagh Ata of the Westernmost Tibetan Plateau. FEMS Microbiology Ecology, 93(7): fix085.  https://doi.org/10.1093/femsec/fix085 Google Scholar
  28. Liu, X. B., Yao, T. D., Kang, S. C., et al., 2010. Bacterial Community of the Largest Oligosaline Lake, Namco on the Tibetan Plateau. Geomicrobiology Journal, 27(8): 669–682.  https://doi.org/10.1080/01490450903528000 Google Scholar
  29. Liu, Y. Q., Priscu, J. C., Yao, T. D., et al., 2014. A Comparison of Pelagic, Littoral, and Riverine Bacterial Assemblages in Lake Bangongco, Tibetan Plateau. FEMS Microbiology Ecology, 89(2): 211–221.  https://doi.org/10.1111/1574-6941.12278 Google Scholar
  30. Liu, Y. Q., Yao, T. D., Jiao, N. Z., et al., 2013a. Seasonal Dynamics of the Bacterial Community in Lake Namco, the Largest Tibetan Lake. Geomicrobiology Journal, 30(1): 17–28.  https://doi.org/10.1080/01490451.2011.638700 Google Scholar
  31. Liu, Y. Q., Yao, T. D., Jiao, N. Z., et al., 2013b. Salinity Impact on Bacterial Community Composition in Five High-Altitude Lakes from the Tibetan Plateau, Western China. Geomicrobiology Journal, 30(5): 462–469.  https://doi.org/10.1080/01490451.2012.710709 Google Scholar
  32. Liu, Y. Q., Yao, T. D., Zhu, L. P., et al., 2009. Bacterial Diversity of Freshwater Alpine Lake Puma Yumco on the Tibetan Plateau. Geomicrobiology Journal, 26(2): 131–145.  https://doi.org/10.1080/01490450802660201 Google Scholar
  33. Llirós, M., Inceoğlu, Ö., García-Armisen, T., et al., 2014. Bacterial Community Composition in Three Freshwater Reservoirs of Different Alkalinity and Trophic Status. PLOS ONE, 9(12): e116145.  https://doi.org/10.1371/journal.pone.0116145 Google Scholar
  34. Margesin, R., Miteva, V., 2011. Diversity and Ecology of Psychrophilic Microorganisms. Research in Microbiology, 162(3): 346–361.  https://doi.org/10.1016/j.resmic.2010.12.004 Google Scholar
  35. Nedwell, D., 1999. Effect of Low Temperature on Microbial Growth: Lowered Affinity for Substrates Limits Growth at Low Temperature. FEMS Microbiology Ecology, 30(2): 101–111.  https://doi.org/10.1016/s0168-6496(99)00030-6 Google Scholar
  36. Nelson, C. E., 2009. Phenology of High-Elevation Pelagic Bacteria: The Roles of Meteorologic Variability, Catchment Inputs and Thermal Stratification in Structuring Communities. The ISME Journal, 3(1): 13–30.  https://doi.org/10.1038/ismej.2008.81 Google Scholar
  37. Newton, R. J., Jones, S. E., Eiler, A., et al., 2011. A Guide to the Natural History of Freshwater Lake Bacteria. Microbiology and Molecular Biology Reviews, 75(1): 14–49.  https://doi.org/10.1128/mmbr.00028-10 Google Scholar
  38. Oren, A., 2001. The Bioenergetic Basis for the Decrease in Metabolic Diversity at Increasing Salt Concentrations: Implications for the Functioning of Salt Lake Ecosystems. Hydrobiologia, 466: 61–72.Google Scholar
  39. Peter, H., Sommaruga, R., 2016. Shifts in Diversity and Function of Lake Bacterial Communities Upon Glacier Retreat. The ISME Journal, 10(7): 1545–1554.  https://doi.org/10.1038/ismej.2015.245 Google Scholar
  40. Qiu, J., 2008. China: The Third Pole. Nature, 454(7203): 393–396.  https://doi.org/10.1038/454393a Google Scholar
  41. Sahay, H., Babu, B. K., Singh, S., et al., 2013. Cold-Active Hydrolases Producing Bacteria from Two Different Sub-Glacial Himalayan Lakes. Journal of Basic Microbiology, 53(8): 703–714.  https://doi.org/10.1002/jobm.201200126 Google Scholar
  42. Sánchez-Hernández, J., Cobo, F., Amundsen, P. A., 2015. Food Web Topology in High Mountain Lakes. PLOS ONE, 10(11): e0143016.  https://doi.org/10.1371/journal.pone.0143016 Google Scholar
  43. Shen, L., Yao, T. D., Xu, B. Q., et al., 2012. Variation of Culturable Bacteria along Depth in the East Rongbuk Ice Core, Mt. Everest. Geoscience Frontiers, 3(3): 327–334.  https://doi.org/10.1016/j.gsf.2011.12.013 Google Scholar
  44. Shokralla, S., Spall, J. L., Gibson, J. F., et al., 2012. Next-Generation Sequencing Technologies for Environmental DNA Research. Molecular Ecology, 21(8): 1794–1805.  https://doi.org/10.1111/j.1365-294x.2012.05538.x Google Scholar
  45. Sogin, M. L., Morrison, H. G., Huber, J. A., et al., 2006. Microbial Diversity in the Deep Sea and the Underexplored “Rare Biosphere”. Proceedings of the National Academy of Sciences, 103(32): 12115–12120.  https://doi.org/10.1073/pnas.0605127103 Google Scholar
  46. Sommaruga, R., 2001. The Role of Solar UV Radiation in the Ecology of Alpine Lakes. Journal of Photochemistry and Photobiology B: Biology, 62(1/2): 35–42.  https://doi.org/10.1016/s1011-1344(01)00154-3 Google Scholar
  47. Sommaruga, R., Casamayor, E. O., 2009. Bacterial ‘Cosmopolitanism’ and Importance of Local Environmental Factors for Community Composition in Remote High-Altitude Lakes. Freshwater Biology, 54(5): 994–1005.  https://doi.org/10.1111/j.1365-2427.2008.02146.x Google Scholar
  48. Stahl, D. A., 1995. Application of Phylogenetically Based Hybridization Probes to Microbial Ecology. Molecular Ecology, 4(5): 535–542.  https://doi.org/10.1111/j.1365-294x.1995.tb00254.x Google Scholar
  49. Stahl, D. A., Flesher, B., Mansfield, H. R., et al., 1988. Use of Phylogenetically Based Hybridization Probes for Studies of Ruminal Microbial Ecology. Applied and Environmental Microbiology, 54(5): 1079–1084.  https://doi.org/10.1002/bit.260310818 Google Scholar
  50. Staley, C., Unno, T., Gould, T. J., et al., 2013. Application of Illumina Next-Generation Sequencing to Characterize the Bacterial Community of the Upper Mississippi River. Journal of Applied Microbiology, 115(5): 1147–1158.  https://doi.org/10.1111/jam.12323 Google Scholar
  51. Thomas, F., Hehemann, J. H., Rebuffet, E., et al., 2011. Environmental and Gut Bacteroidetes: The Food Connection. Frontiers in Microbiology, 2(5): 1–16.  https://doi.org/10.3389/fmicb.2011.00093 Google Scholar
  52. Tuomisto, H., 2012. An Updated Consumer’s Guide to Evenness and Related Indices. Oikos, 121(8): 1203–1218.  https://doi.org/10.1111/j.1600-0706.2011.19897.x Google Scholar
  53. Wang, J. J., Yang, D. M., Zhang, Y., et al., 2011. Do Patterns of Bacterial Diversity along Salinity Gradients Differ from Those Observed for Macroorganisms?. PLOS ONE, 6(11): e27597.  https://doi.org/10.1371/journal.pone.0027597 Google Scholar
  54. Wang, P. F., Wang, X., Wang, C., et al., 2017. Shift in Bacterioplankton Diversity and Structure: Influence of Anthropogenic Disturbances along the Yarlung Tsangpo River on the Tibetan Plateau, China. Scientific Reports, 7(1): 12529.  https://doi.org/10.1038/s41598-017-12893-4 Google Scholar
  55. Wang, Q., Garrity, G. M., Tiedje, J. M., et al., 2007. Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy. Applied and Environmental Microbiology, 73(16): 5261–5267.  https://doi.org/10.1128/aem.00062-07 Google Scholar
  56. Ward, D. M., Weller, R., Bateson, M. M., 1990. 16S rRNA Sequences Reveal Numerous Uncultured Microorganisms in a Natural Community. Nature, 345(6270): 63–65.  https://doi.org/10.1038/345063a0 Google Scholar
  57. Warnecke, F., Sommaruga, R., Sekar, R., et al., 2005. Abundances, Identity, and Growth State of Actinobacteria in Mountain Lakes of Different UV Transparency. Applied and Environmental Microbiology, 71(9): 5551–5559.  https://doi.org/10.1128/aem.71.9.5551-5559.2005 Google Scholar
  58. Williamson, C. E., Dodds, W., Kratz, T. K., et al., 2008. Lakes and Streams as Sentinels of Environmental Change in Terrestrial and Atmospheric Processes. Frontiers in Ecology and the Environment, 6(5): 247–254.  https://doi.org/10.1890/070140 Google Scholar
  59. Wu, Q. L., Zwart, G., Schauer, M., et al., 2006. Bacterioplankton Community Composition along a Salinity Gradient of Sixteen High-Mountain Lakes Located on the Tibetan Plateau, China. Applied and Environmental Microbiology, 72(8): 5478–5485.  https://doi.org/10.1128/aem.00767-06 Google Scholar
  60. Xing, P., Hahn, M. W., Wu, Q. L., 2009. Low Taxon Richness of Bacterioplankton in High-Altitude Lakes of the Eastern Tibetan Plateau, with a Predominance of Bacteroidetes and Synechococcus Spp.. Applied and Environmental Microbiology, 75(22): 7017–7025.  https://doi.org/10.1128/aem.01544-09 Google Scholar
  61. Xiong, J. B., Liu, Y. Q., Lin, X. G., et al., 2012. Geographic Distance and pH Drive Bacterial Distribution in Alkaline Lake Sediments across Tibetan Plateau. Environmental Microbiology, 14(9): 2457–2466.  https://doi.org/10.1111/j.1462-2920.2012.02799.x Google Scholar
  62. Yadav, A. N., Sachan, S. G., Verma, P., et al., 2016. Cold Active Hydrolytic Enzymes Production by Psychrotrophic Bacilli Isolated from Three Sub-Glacial Lakes of NW Indian Himalayas. Journal of Basic Microbiology, 56(3): 294–307.  https://doi.org/10.1002/jobm.201500230 Google Scholar
  63. Yang, J., Ma, L., Jiang, H. C., et al., 2016. Salinity Shapes Microbial Diversity and Community Structure in Surface Sediments of the Qinghai-Tibetan Lakes. Scientific Reports, 6(1): 25078.  https://doi.org/10.1038/srep25078 Google Scholar
  64. Yannarell, A. C., Triplett, E. W., 2005. Geographic and Environmental Sources of Variation in Lake Bacterial Community Composition. Applied and Environmental Microbiology, 71(1): 227–239.  https://doi.org/10.1128/aem.71.1.227-239.2005 Google Scholar
  65. Yao, T. D., Thompson, L. G., Mosbrugger, V., et al., 2012. Third Pole Environment (TPE). Environmental Development, 3(1): 52–64.  https://doi.org/10.1016/j.envdev.2012.04.002 Google Scholar
  66. Zhang, G. Q., Yao, T. D., Xie, H. J., et al., 2015. An Inventory of Glacial Lakes in the Third Pole Region and Their Changes in Response to Global Warming. Global and Planetary Change, 131(6): 148–157.  https://doi.org/10.1016/j.gloplacha.2015.05.013 Google Scholar
  67. Zhang, Q., Hou, X. Y., Li, F. Y., et al., 2014. Alpha, Beta and Gamma Diversity Differ in Response to Precipitation in the Inner Mongolia Grassland. PLOS ONE, 9(3): e93518.  https://doi.org/10.1371/journal.pone.0093518 Google Scholar
  68. Zhang, R., Wu, Q. L., Piceno, Y. M., et al., 2013. Diversity of Bacterioplankton in Contrasting Tibetan Lakes Revealed by High-Density Microarray and Clone Library Analysis. FEMS Microbiology Ecology, 86(2): 277–287.  https://doi.org/10.1111/1574-6941.12160 Google Scholar
  69. Zhang, S., Hou, S., Wu, Y., et al., 2008. Bacterial Diversity in Himalayan Glacial Ice and Its Relationship to Dust. Biogeosciences Discussions, 5(4): 3433–3456.  https://doi.org/10.5194/bgd-5-3433-2008 Google Scholar
  70. Zhong, Z. P., Liu, Y., Miao, L. L., et al., 2016. Prokaryotic Community Structure Driven by Salinity and Ionic Concentrations in Plateau Lakes of the Tibetan Plateau. Applied and Environmental Microbiology, 82(6): 1846–1858.  https://doi.org/10.1128/aem.03332-15 Google Scholar
  71. Zwart, G., Crump, B. C., Agterveld, M. P. K., et al., 2002. Typical Freshwater Bacteria: An Analysis of Available 16S rRNA Gene Sequences from Plankton of Lakes and Rivers. Aquatic Microbial Ecology, 28: 141–155.  https://doi.org/10.3354/ame028141 Google Scholar

Copyright information

© China University of Geosciences (Wuhan) and Springer-Verlag GmbH Germany, Part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Alpine Ecology and Biodiversity, Institute of Tibetan Plateau ResearchChinese Academy of SciencesBeijingChina
  2. 2.Key Laboratory of Tibetan Environment Changes and Land Surface Processes, Institute of Tibetan Plateau ResearchChinese Academy of SciencesBeijingChina
  3. 3.University of Chinese Academy of ScienceBeijingChina
  4. 4.Janapriya Multiple CampusTribhuvan UniversityPokharaNepal
  5. 5.Kathmandu Center for Research and EducationCAS-TUKathmanduNepal

Personalised recommendations