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First report on the bacterial community composition, diversity, and functions in Ramsar site of Central Himalayas, Nepal

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Abstract

Wetland bacterial communities are highly sensitive to altered hydrology and the associated change in water physicochemical and biological properties leading to shifts in community composition and diversity, hence affecting the ecological roles. However, relevant studies are lacking in the wetlands of central Himalayas Nepal. Thus, we aimed to explore the variation of bacterial communities, diversity, and ecologic functions in the wet and dry periods of a wetland (designed as Ramsar site, Ramsar no 2257) by using 16S rRNA gene-based Illumina MiSeq sequencing. We reported a pronounced variation in water physicochemical and biological properties (temperature, pH, Chla, DOC, and TN), bacterial diversity, and community composition. Bacterial communities in the dry season harbored significantly higher alpha diversity, while significantly higher richness and abundance were reflected in the wet season. Our results uncovered the effect of nutrients on bacterial abundance, richness, and community composition. Fourteen percent of the total OTUs were shared in two hydrological periods, and the largest portion of unique OTUs (58%) was observed in the dry season. Planctomycetes and Bacteroidetes dominated the wet season exclusive OTUs; meanwhile, Actinobacteria dominated the dry season exclusive OTUs. Bacteria in these wetlands exhibited divergent ecological functions during the dry and wet seasons. By disclosing the variation of water bacterial communities in different hydrologic periods and their relationship with environmental factors, this first-hand work in the Ramsar site of Nepal will develop a baseline dataset for the scientific community that will assist in understanding the wetland’s microbial ecology and biogeography.

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References

  • Adhikari, N. P., Liu, Y., Liu, K., Zhang, F., Adhikari, S., Chen, Y., & Liu, X. (2019). Bacterial community composition and diversity in Koshi River, the largest river of Nepal. Ecological Indicators, 104(May), 501–511. https://doi.org/10.1016/j.ecolind.2019.05.009

    Article  Google Scholar 

  • Adhikari, S., Zhang, F., Zeng, C., Tripathee, L., Adhikari, N. P., Xu, J., & Wang, G. (2020). Precipitation chemistry and stable isotopic characteristics at Wengguo in the northern slopes of the Himalayas. Journal of Atmospheric Chemistry, 76(4), 289–313. https://doi.org/10.1007/s10874-020-09399-1

    Article  CAS  Google Scholar 

  • Adhikari, S., Zhang, F., Adhikari, N. P., Zeng, C., Pant, R. R., Ram, K., et al. (2021). Atmospheric wet deposition of major ionic constituents and inorganic nitrogen in Bangladesh: implications for spatiotemporal variation and source apportionment. Atmospheric Research, 250(October 2020), 105414. https://doi.org/10.1016/j.atmosres.2020.105414

    Article  CAS  Google Scholar 

  • Allgaier, M., & Grossart, H. P. (2006). Diversity and seasonal dynamics of Actinobacteria populations in four lakes in Northeastern Germany. Applied and Environmental Microbiology, 72(5), 3489–3497. https://doi.org/10.1128/AEM.72.5.3489-3497.2006

    Article  CAS  Google Scholar 

  • Anderson, M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32–46.

    Google Scholar 

  • Andrei, A. Ş, Salcher, M. M., Mehrshad, M., Rychtecký, P., Znachor, P., & Ghai, R. (2019). Niche-directed evolution modulates genome architecture in freshwater Planctomycetes. ISME Journal, 13(4), 1056–1071. https://doi.org/10.1038/s41396-018-0332-5

    Article  Google Scholar 

  • Bondoso, J., Godoy-Vitorino, F., Balagué, V., Gasol, J. M., Harder, J., & Lage, O. M. (2017). Epiphytic Planctomycetes communities associated with three main groups of macroalgae. FEMS Microbiology Ecology, 93(3), 1–9. https://doi.org/10.1093/femsec/fiw255

    Article  CAS  Google Scholar 

  • Boyer, E. W., Howarth, R. W., Galloway, J. N., Dentener, F. J., Green, P. A., & Vörösmarty, C. J. (2006). Riverine nitrogen export from the continents to the coasts. Global Biogeochemical Cycles, 20(1), 1–9. https://doi.org/10.1029/2005GB002537

  • Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5), 335–336. https://doi.org/10.1038/nmeth.f.303.QIIME

    Article  CAS  Google Scholar 

  • Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-lyons, D., Huntley, J., Fierer, N., et al. (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal, 6, 1621–1624. https://doi.org/10.1038/ismej.2012.8

    Article  CAS  Google Scholar 

  • Castro González, M., Pacheco Montealegre, M. E., & Restrepo Benavides, M. (2022). Bacterial communities in sediments of an urban wetland in Bogota, Colombia. Universitas Scientiarum, 27(2), 163–185. https://doi.org/10.11144/javeriana.sc272.bcis

    Article  CAS  Google Scholar 

  • Chen, H., & Boutros, P. C. (2011). VennDiagram: A package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics, 12(1), 35. https://doi.org/10.1186/1471-2105-12-35

    Article  Google Scholar 

  • Crump, B. C., Armbrust, E. V., & Baross, J. A. (1999). Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent Coastal Ocean. Applied and Environmental Microbiology, 65(7), 3192–3204.

    Article  CAS  Google Scholar 

  • Dahal, P., Shrestha, N. S., Shrestha, M. L., Krakauer, N. Y., Panthi, J., Pradhanang, S. M., et al. (2016). Drought risk assessment in central Nepal: Temporal and spatial analysis. Natural Hazards, 80(3), 1913–1932. https://doi.org/10.1007/s11069-015-2055-5

    Article  Google Scholar 

  • Dai, Y., Yang, Y., Wu, Z., Feng, Q., Xie, S., & Liu, Y. (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

    Article  CAS  Google Scholar 

  • Duce, R. A., LaRoche, J., Altieri, K., Arrigo, K. R., Baker, A. R., Capone, D. G., et al. (2008). Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science, 320(5878), 893–897. https://doi.org/10.1126/science.1150369

  • Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26(19), 2460–2461. https://doi.org/10.1093/bioinformatics/btq461

    Article  CAS  Google Scholar 

  • Farjalla, V. F., Azevedo, D. A., Esteves, F. A., Bozelli, R. L., Roland, F., & Enrich-Prast, A. (2006). Influence of hydrological pulse on bacterial growth and DOC uptake in a clear-water Amazonian lake. Microbial Ecology, 52(2), 334–344. https://doi.org/10.1007/s00248-006-9021-4

    Article  Google Scholar 

  • Fisher, J. C., Newton, R. J., Dila, D. K., & McLellan, S. L. (2015). Urban microbial ecology of a freshwater estuary of Lake Michigan. Elementa, 3, 1–14. https://doi.org/10.12952/journal.elementa.000064

    Article  Google Scholar 

  • Gurung, T. B., Dhakal, R. P., Husen, M. A., & Jones, J. R. (2010). Abundance and nutrient limiting growth rate of heterotrophic bacterio-plankton in Himalayan foot hill Lake Phewa, Nepal. Lakes and Reservoirs: Research and Management, 15(1), 53–61. https://doi.org/10.1111/j.1440-1770.2010.00422.x

    Article  CAS  Google Scholar 

  • Hahn, M. W., Lünsdorf, H., Wu, Q., Schauer, M., Höfle, M. G., Boenigk, J., & Stadler, P. (2003). Isolation of novel ultramicrobacteria classified as Actinobacteria from five freshwater habitats in Europe and Asia. Applied and Environmental Microbiology, 69(3), 1442–1451. https://doi.org/10.1128/AEM.69.3.1442-1451.2003

    Article  CAS  Google Scholar 

  • Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontoplogical Statistics Software Package for education and data analysis. Palaeontologia Electronica, 4(1), 1–9.

    Google Scholar 

  • Hedges, J. I., Cowie, G. L., Richey, J. E., Quay, P. D., Benner, R., Strom, M., & Forsberg, B. R. (1994). Origins and processing of organic matter in the Amazon River as indicated by carbohydrates and amino acids. Limnology and Oceanography, 39(4), 743–761. https://doi.org/10.4319/lo.1994.39.4.0743

    Article  CAS  Google Scholar 

  • Kaphle, B., Wang, J. B., Kai, J. L., Lyu, X. M., Paudayal, K. N., & Adhikari, S. (2021). Hydrochemistry of Rara Lake: a Ramsar lake from the southern slope of the central Himalayas, Nepal. Journal of Mountain Science, 18(1), 141–158. https://doi.org/10.1007/s11629-019-5910-0

    Article  Google Scholar 

  • Khadka, U. R., & Ramanathan, A. L. (2013). Major ion composition and seasonal variation in the Lesser Himalayan lake: Case of Begnas Lake of the Pokhara Valley, Nepal. Arabian Journal of Geosciences, 6(11), 4191–4206. https://doi.org/10.1007/s12517-012-0677-4

    Article  CAS  Google Scholar 

  • Kirchman, D. L. (2002). The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiology Ecology, 39, 91–100.

    CAS  Google Scholar 

  • Kistemann, T., Claßen, T., Koch, C., Dangendorf, F., Fischeder, R., Gebel, J., et al. (2002). Microbial load of drinking water reservoir tributaries during extreme rainfall and runoff. Applied and Environmental Microbiology, 68(5), 2188–2197. https://doi.org/10.1128/AEM.68.5.2188-2197.2002

    Article  CAS  Google Scholar 

  • Kong, Z., Kou, W., Ma, Y., Yu, H., Ge, G., & Wu, L. (2018). Seasonal dynamics of the bacterioplankton community in a large, shallow, highly dynamic freshwater lake. Canadian Journal of Microbiology, 797(May), 786–797.

    Article  Google Scholar 

  • Landa, M., Blain, S., Christaki, U., Monchy, S., & Obernosterer, I. (2016). Shifts in bacterial community composition associated with increased carbon cycling in a mosaic of phytoplankton blooms. ISME Journal, 10(1), 39–50. https://doi.org/10.1038/ismej.2015.105

  • Lindström, E. S., Agterveld, M. P. K., Zwart, G., Kamst-Van Agterveld, M. P., & Zwart, G. (2005). Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time 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

    Article  Google Scholar 

  • Liu, K., Liu, Y., Jiao, N., Xu, B., Gu, Z., Xing, T., & Xiong, J. (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), 1-9. https://doi.org/10.1093/femsec/fix085.

  • Louca, S., Parfery, L. W., & Doebeli, M. (2016). Decoupling function and taxonomy in the global ocean microbiome. Science, 353(6305), 1272–1277. https://doi.org/10.1126/science.aaf4507

    Article  CAS  Google Scholar 

  • Ma, Y., Li, J., Wu, J., Kong, Z., Feinstein, L. M., Ding, X., et al. (2018). Bacterial and fungal community composition and functional activity associated with lake wetland water level gradients. Scientific Reports, 8(1), 1–12. https://doi.org/10.1038/s41598-018-19153-z

    Article  CAS  Google Scholar 

  • MacFarland T.W., Y. J. M. (2016). Kruskal–Wallis H-test for oneway analysis of variance (ANOVA) by ranks. In Introduction to Nonparametric Statistics for the Biological Sciences Using R. Springer, Cham. https://doi.org/10.1007/978-3-319-30634-6

  • Magoˇc, T., & Salzberg, S. L. (2011). FLASH : Fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27(21), 2957–2963. https://doi.org/10.1093/bioinformatics/btr507

    Article  CAS  Google Scholar 

  • 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/10.1111/j.1574-6941.1999.tb00639.x

    Article  CAS  Google Scholar 

  • Needham, D. M., & Fuhrman, J. A. (2016). Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom. Nature Microbiology, 1(4), 1–7. https://doi.org/10.1038/nmicrobiol.2016.5

    Article  CAS  Google Scholar 

  • Newton, R. J., Jones, S. E., Eiler, A., McMahon, K. D., & Bertilsson, S. (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

    Article  CAS  Google Scholar 

  • Panthi, J., Dahal, P., Shrestha, M., Aryal, S., Krakauer, N., Pradhanang, S., et al. (2015). Spatial and temporal variability of rainfall in the Gandaki River Basin of Nepal Himalaya. Climate, 3(1), 210–226. https://doi.org/10.3390/cli3010210

    Article  Google Scholar 

  • Paudel, N., Adhikari, S., & Paudel, G. (2017). Ramsar lakes in the foothills of Himalaya, Pokhara- Lekhnath, Nepal : An overview. Janapriya Journal of Interdisciplinary Studies, 6, 134–147.

    Article  Google Scholar 

  • Regalado, N. G., Martin, G., & Antony, S. J. (2009). Acinetobacter lwoffii: Bacteremia associated with acute gastroenteritis. Travel Medicine and Infectious Disease, 7(5), 316–317. https://doi.org/10.1016/j.tmaid.2009.06.001

    Article  Google Scholar 

  • Ren, Z., Qu, X., Zhang, M., Yu, Y., & Peng, W. (2019). Distinct bacterial communities in wet and dry seasons during a seasonal water level fluctuation in the largest freshwater lake (Poyang Lake) in China. Frontiers in Microbiology, 10(1167), 1–13. https://doi.org/10.3389/fmicb.2019.01167

    Article  Google Scholar 

  • Salimi, S., Almuktar, S. A. A. A. N., & Scholz, M. (2021). Impact of climate change on wetland ecosystems : a critical review of experimental wetlands. Journal of Environmental Management, 286(August 2020), 112160. https://doi.org/10.1016/j.jenvman.2021.112160

    Article  CAS  Google Scholar 

  • Sánchez, M. B. (2015). Antibiotic resistance in the opportunistic pathogen Stenotrophomonas maltophilia. Frontiers in Microbiology, 6(JUN), 1–7. https://doi.org/10.3389/fmicb.2015.00658

    Article  Google Scholar 

  • Sanchez, G. (2013). PLS Path Modeling with R. Berkeley; Trowchez Editions, 2013.

  • Sansupa, C., Wahdan, S. F. M., Hossen, S., Disayathanoowat, T., Wubet, T., & Purahong, W. (2021). Can we use functional annotation of prokaryotic taxa (Faprotax) to assign the ecological functions of soil bacteria? Applied Sciences (switzerland), 11(2), 1–17. https://doi.org/10.3390/app11020688

    Article  CAS  Google Scholar 

  • Shahraki, A. H., Chaganti, S. R., Heath, D., & Clair, L. S. (2021). Spatio-temporal dynamics of bacterial communities in the. BMC Microbiology, 21(253), 1–15.

    Google Scholar 

  • Sigee, D. C. (2005). Freshwater microbiology. John Wiley & Sons Ltd, The Atrium, Southern Gate, Chichester, West Sussex PO19 8SQ, England.

  • Søndergaard, M., & Theil-Nielsen, J. (1997). Bacterial growth efficiency in lakewater cultures. Aquatic Microbial Ecology, 12(2), 115–122. https://doi.org/10.3354/ame012115

  • Staley, C., Unno, T., Gould, T. J., Jarvis, B., Phillips, J., Cotner, J. B., & Sadowsky, M. J. (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

    Article  CAS  Google Scholar 

  • Sun, Y., Li, X., Liu, J., Yao, Q., Jin, J., Liu, X., & Wang, G. (2019). Comparative analysis of bacterial community compositions between sediment and water in different types of wetlands of northeast China. Journal of Soils and Sediments, 19: 3083–3097. https://doi.org/10.1007/s11368-019-02301-x.

  • Tadonléké, R. D. (2007). Strong coupling between natural Planctomycetes and changes in the quality of dissolved organic matter in freshwater samples. FEMS Microbiology Ecology, 59(3), 543–555. https://doi.org/10.1111/j.1574-6941.2006.00222.x

    Article  CAS  Google Scholar 

  • Team, R. C. (2014). R: A language and environment for statistical computing. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. R Foundation for Statistical Computing, Vienna, Austria. https://doi.org/10.1530/EJE-14-0355

  • Wang, J., Feiyan, P., Soininen, J., Heino, J., & Shen, J. (2016). Nutrient enrichment modifies temperature-biodiversity relationships in large-scale field experiments. Nature Communications, 7(December), 1–9. https://doi.org/10.1038/ncomms13960

    Article  CAS  Google Scholar 

  • Wang, B., Zheng, X., Zhang, H., Xiao, F., Gu, H., Zhang, K., et al. (2020). Bacterial community responses to tourism development in the Xixi National Wetland Park China. Science of the Total Environment, 20, 137570. https://doi.org/10.1016/j.scitotenv.2020.137570

    Article  CAS  Google Scholar 

  • Weiss, M., & Simon, M. (1999). Consumption of labile dissolved organic matter by limnetic bacterioplankton: The relative significance of amino acids and carbohydrates. Aquatic Microbial Ecology, 17(1), 1–12. https://doi.org/10.3354/ame017001

  • Wiegand, S., Jogler, M., & Jogler, C. (2018). On the maverick Planctomycetes. FEMS Microbiology Reviews, 42(6), 739–760. https://doi.org/10.1093/femsre/fuy029

    Article  CAS  Google Scholar 

  • Williamson, C. E., Dodds, W., Kratz, T. K., & Palmer, M. A. (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

  • Xia, X., Zhang, S., Li, S., Zhang, L., Wang, G., Zhang, L., et al. (2018). The cycle of nitrogen in river systems: Sources, transformation, and flux. Environmental Science: Processes and Impacts, 20(6), 863–891. https://doi.org/10.1039/c8em00042e

  • Xu, H., Zhao, D., Huang, R., Cao, X., Zeng, J., Yu, Z., et al. (2018). Contrasting network features between free-living and particle-attached bacterial communities in Taihu Lake. Microbial Ecology, 76(2), 303–313. https://doi.org/10.1007/s00248-017-1131-7

    Article  Google Scholar 

  • Yang, Y., Hou, Y., Ma, M., & Zhan, A. (2019). Potential pathogen communities in highly polluted river ecosystems: Geographical distribution and environmental influence. Ambio. https://doi.org/10.1007/s13280-019-01184-z

    Article  Google Scholar 

  • Yi, X., Ning, C., Feng, S., Gao, H., Zhao, J., Liao, J. et al., (2022). Urbanization-induced environmental changes strongly affect wetland soil bacterial community composition and diversity. Environmental Research Letters, 17(2022) 014027. https://doi.org/10.1088/1748-9326/ac444f.

  • Zedler, J. B., & Kercher, S. (2005). Wetland resources: status, trends, ecosystem services, and restorability. Annual Review of Environment and Resources, 30, 39–74. https://doi.org/10.1146/annurev.energy.30.050504.144248 

  • Zhao, J., Shu, W., Wang, L., & Zhang, X. (2022). Limnologica severe drought changes the soil bacterial community in wetland ecosystem : evidence from the largest freshwater lake wetland in China. Limnologica, 97(February), 126023. https://doi.org/10.1016/j.limno.2022.126023

    Article  CAS  Google Scholar 

  • Zhao, D., Xu, H., Zeng, J., Cao, X., Huang, R., Shen, F., & Yu, Z. (2017). Community composition and assembly processes of the free-living and particle-attached bacteria in Taihu Lake. FEMS Microbiology Ecology, 93, 1–10. https://doi.org/10.1093/femsec/fix062

    Article  CAS  Google Scholar 

  • Zhi, E., Song, Y., Duan, L., Yu, H., & Peng, J. (2015). Spatial distribution and diversity of microbial community in large-scale constructed wetland of the Liao River Conservation Area. Environmental Earth Sciences, 73(9), 5085–5094. https://doi.org/10.1007/s12665-015-4021-7

    Article  Google Scholar 

  • Zhu, X., Wang, L., Zhang, X., He, M., Wang, D., Ren, Y., et al. (2022). Effects of different types of anthropogenic disturbances and natural wetlands on water quality and microbial communities in a typical black-odor river. Ecological Indicators, 136, 108613. https://doi.org/10.1016/j.ecolind.2022.108613

    Article  CAS  Google Scholar 

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Funding

The Second Tibetan Plateau Scientific Expedition and Research (STEP) program (Grant No.2019QZKK0503) and the National Natural Science Foundation of China (Grant No. U21A20176) financially supported this work. Namita Paudel Adhikari was supported by CAS-TWAS President’s Fellowship Program (Award no: 20190365) for Ph.D.

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Study design: Namita Paudel Adhikari. Collection and processing of samples: Subash Adhikari. Experimental work: Namita Paudel Adhikari. Bioinformatics and statistical analysis: Namita Paudel Adhikari, Subash Adhikari. Interpretation of the data: Namita Paudel Adhikari. Drafting and revision of the manuscript: Namita Paudel Adhikari and Subash Adhikari.

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Adhikari, N.P., Adhikari, S. First report on the bacterial community composition, diversity, and functions in Ramsar site of Central Himalayas, Nepal. Environ Monit Assess 195, 573 (2023). https://doi.org/10.1007/s10661-023-11158-0

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