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Genetic diversity patterns of microbial communities in a subtropical riverine ecosystem (Jiulong River, southeast China)

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Abstract

Prokaryotic and eukaryotic microbes are key organisms in aquatic ecosystems and play pivotal roles in the biogeochemical cycles, but little is known about genetic diversity of these communities in subtropical rivers. In this study, microbial planktonic communities were determined by using denaturing gradient gel electrophoresis (DGGE) analysis from the Jiulong River, southeast China, and their relationships with local environmental factors were studied. The Betaproteobacteria (26%) and Dinophyceae (26%) were the most dominant taxa in prokaryotic and eukaryotic clones derived from DGGE bands, respectively. Further, both cluster and ordination analyses of prokaryotic and eukaryotic DGGE fingerprinting resulted in three identical groups from the 15 sites, which were closely related with the environmental factors. Partial redundancy analysis (partial RDA) revealed that agricultural pollution (phosphorus and nitrogen) and saltwater intrusion (conductivity and salinity) were the main factors impacting microbial community composition, by explaining more than two-thirds of the total variation in both prokaryotic (67.0%) and eukaryotic (70.5%) communities. Moreover, the robust and quantifiable relationship between DGGE results and environmental variables indicated that the community-level molecular fingerprinting techniques could support the physicochemical assessment of riverine water quality and ecosystem health.

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References

  • Amann, R. I., W. Ludwig & K. H. Schleifer, 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiological Reviews 59: 143–169.

    PubMed  CAS  Google Scholar 

  • Anderson, D. M., 1989. Toxic algal blooms and red tides: a global perspective. In Ochaichi, R., D. M. Anderson & T. Nemoto (eds), Red Tides: Biology, Environmental Science and Toxicology. Proceedings of the First International Symposium, Red Tides, Japan, 1987. Elsevier, New York: 11–16.

  • Anderson, D. M. & K. D. Stolzenbach, 1985. Selective retention of two dinoflagellates in a well-mixed estuarine embayment: the importance of diel vertical migration and surface avoidance. Marine Ecology Progress Series 25: 39–50.

    Article  Google Scholar 

  • Bernhard, A. E., D. Colbert, J. McManus & K. G. Field, 2005. Microbial community dynamics based on 16S rRNA gene profiles in a Pacific Northwest estuary and its tributaries. FEMS Microbiology Ecology 52: 115–128.

    Article  PubMed  CAS  Google Scholar 

  • Caron, D. A., R. J. Gast, E. L. Lim & M. R. Dennett, 1999. Protistan community structure: molecular approaches for answering ecological questions. Hydrobiologia 401: 215–227.

    Article  Google Scholar 

  • Clarke, K. R. & R. N. Gorley, 2001. PRIMER v5: User Manual/Tutorial. PRIMER-E, Plymouth.

    Google Scholar 

  • Cody, D. G., R. T. Heath & L. G. Leff, 2000. Characterization benthic bacterial assemblages in a polluted stream using denaturing gradient gel electrophoresis. Hydrobiologia 432: 207–215.

    Article  Google Scholar 

  • Crump, B. C., E. V. Armbrust & J. A. Baross, 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: 3192–3204.

    PubMed  CAS  Google Scholar 

  • Crump, B. C., C. S. Hopkinson, M. L. Sogin & J. E. Hobbie, 2004. Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Applied and Environmental Microbiology 70: 1494–1505.

    Article  PubMed  CAS  Google Scholar 

  • Danovaro, R., G. M. Luna, A. Dell’Anno & B. Pietrangeli, 2006. Comparison of two fingerprinting techniques, terminal restriction fragment length polymorphism and automated ribosomal intergenic spacer analysis, for determination of bacterial diversity in aquatic environments. Applied and Environmental Microbiology 72: 5982–5989.

    Article  PubMed  CAS  Google Scholar 

  • Diez, B., C. Pedros-Alio, T. L. Marsh & R. Massana, 2001. Application of denaturing gradient gel electrophoresis (DGGE) to study the diversity of marine picoeukaryotic assemblages and comparison of DGGE with other molecular techniques. Applied and Environmental Microbiology 67: 2942–2951.

    Article  PubMed  CAS  Google Scholar 

  • Guan, H. S., W. P. Wang, Q. S. Jiang, H. S. Hong & L. P. Zhang, 2005. A statistical model for evaluating water pollution in Jiulong River Watershed. Environmental Informatics Archives 3: 185–192.

    Google Scholar 

  • Hahn, M. W., H. Luensdorf, Q. Wu, M. Schauer, M. G. Hoefle, J. Boenigk & P. Stadler, 2003. Isolation of novel ultramicrobacteria classified as Actinobacteria from five freshwater habitats in Europe and Asia. Applied and Environmental Microbiology 69: 1442–1451.

    Article  PubMed  CAS  Google Scholar 

  • Hallegraeff, G. M., 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32: 79–99.

    Article  Google Scholar 

  • Hewson, I. & J. A. Fuhrman, 2004. Richness and diversity of bacterioplankton species along an estuarine gradient in Moreton Bay, Australia. Applied and Environmental Microbiology 70: 3425–3433.

    Article  PubMed  CAS  Google Scholar 

  • Horne, A. J. & R. Goldman, 1994. Estuaries. In Horne, A. J. & C. R. Goldman (eds), Limnology. McGraw-Hill, New York: 433–456.

    Google Scholar 

  • Iliopoulou-Georgudaki, J., V. Kantzaris, P. Katharios, P. Kaspiris, T. Georgiadis & B. Montesantou, 2003. An application of different bioindicators for assessing water quality: a case study in the rivers Alfeios and Pineios (Peloponnisos, Greece). Ecological Indicators 2: 345–360.

    Article  CAS  Google Scholar 

  • Jiang, J. G. & Y. F. Shen, 2007. Development of the microbial communities in Lake Donghu in relation to water quality. Environmental Monitoring and Assessment 127: 227–236.

    Article  PubMed  CAS  Google Scholar 

  • Kent, A. D., S. E. Jones, G. H. Lauster, J. M. Graham, R. J. Newton & K. D. McMahon, 2006. Experimental manipulations of microbial food web interactions in a humic lake: shifting biological drivers of bacterial community structure. Environmental Microbiology 8: 1448–1459.

    Article  PubMed  CAS  Google Scholar 

  • Kruskal, J. B., 1964. Multi-dimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29: 1–27.

    Article  Google Scholar 

  • Lan, D. Z., Q. Fang, H. F. Gu & C. Li, 2004. Resting cysts of harmful and toxic dinoflagellates and potential damage of Alexandrium tamarense from Xiamen Bay sediments. Journal of Oceanography in Taiwan Strait 23: 453–457. (in Chinese).

    Google Scholar 

  • Laybourn-Parry, J., 1992. Protozoan Plankton Ecology. Chapman and Hall, London.

    Google Scholar 

  • Leff, L. G., 2002. Stream microbiology. In Bitton, G. (ed.), Encyclopedia of Environmental Microbiology. John Wiley and Sons, Inc., NewYork: 3015–3024.

    Google Scholar 

  • Litaker, R. W., P. A. Tester, C. S. Duke, B. E. Kenney, J. L. Pinckney & J. Ramus, 2002. Seasonal niche strategy of the bloom-forming dinoflagellate Heterocapsa triquetra. Marine Ecology Progress Series 232: 45–62.

    Article  Google Scholar 

  • Lu, S. & I. J. Hodgkiss, 2004. Harmful algal bloom causative collected from Hong Kong waters. Hydrobiologia 512: 231–238.

    Article  Google Scholar 

  • Muyzer, G., 1999. DGGE/TGGE a method for identifying genes from natural ecosystems. Current Opinion in Microbiology 2: 317–322.

    Article  PubMed  CAS  Google Scholar 

  • Okubo, A. & S. Sugiyama, 2009. Comparison of molecular fingerprinting methods for analysis of soil microbial community structure. Ecological Research 24: 1399–1405.

    Article  Google Scholar 

  • Passy, S. I., 2007. Community analysis in stream biomonitoring: what we measure and what we don’t. Environmental Monitoring and Assessment 127: 409–417.

    Article  PubMed  CAS  Google Scholar 

  • Pedros-Alio, C., J. I. Calderon-Paz, M. H. MacLean, G. Medina, C. Marrase, J. M. Gasol & N. Guixa-Boixereu, 2000. The microbial food web along salinity gradients. FEMS Microbiology Ecology 32: 143–155.

    Article  PubMed  CAS  Google Scholar 

  • Pernthaler, J., T. Posch, K. Simek, J. Vrba, A. Pernthaler, F. O. Gloeckner, U. Nuebel, R. Psenner & R. Amann, 2001. Predator-specific enrichment of Actinobacteria from a cosmopolitan freshwater clade in mixed continuous culture. Applied and Environmental Microbiology 67: 2145–2155.

    Article  PubMed  CAS  Google Scholar 

  • Pomeroy, L. R., P. J. L. B. Williams, F. Azam & J. E. Hobbie, 2007. The microbial loop. Oceanography 20(2): 28–33.

    Article  Google Scholar 

  • Potapova, M. G. & D. F. Charles, 2002. Benthic diatoms in USA rivers: distributions along spatial and environmental gradients. Journal of Biogeography 29: 167–187.

    Article  Google Scholar 

  • Reynolds, C. S., 1984. Phytoplankton periodicity: the interaction of form, function and environmental variability. Freshwater Biology 14: 111–142.

    Article  Google Scholar 

  • Sakami, T., 2008. Seasonal and spatial variation of bacterial community structure in river-mouth areas of Gokasho Bay, Japan. Microbes and Environments 23: 277–284.

    Article  PubMed  Google Scholar 

  • Santos, H. F., J. C. Cury, F. L. Carmo, A. S. Rosado & R. S. Peixoto, 2010. 18S rDNA sequences from microeukaryotes reveal oil indicators in mangrove sediment. PLoS ONE 5(8): e12437. doi:10.1371/journal.pone.0012437.

    Article  PubMed  Google Scholar 

  • Schäfer, H. & G. Muyzer, 2001. Denaturing gradient gel electrophoresis in marine microbial ecology. In Paul, J. H. (ed.), Methods in Microbiology, Vol. 30. Academic Press, London: 425–468.

    Google Scholar 

  • Schauer, M., R. Massana & C. Pedros-Alio, 2000. Spatial differences in bacterioplankton composition along the Catalan coast (NW Mediterranean) assessed by molecular fingerprinting. FEMS Microbiology Ecology 33: 51–59.

    Article  PubMed  CAS  Google Scholar 

  • Sekiguchi, H., M. Watanabe, T. Nakahara, B. Xu & H. Uchiyama, 2002. Succession of bacterial community structure along the Changjiang River determined by denaturing gradient gel electrophoresis and clone library analysis. Applied and Environmental Microbiology 68: 5142–5150.

    Article  PubMed  CAS  Google Scholar 

  • Stepanauskas, R. N., V. F. Farjalla, L. J. Tranvik, J. M. Svensson, F. A. Esteves & W. Granéli, 2000. Bioavailability and sources of DOC and DON in macrophyte stands of a tropical coastal lake. Hydrobiologia 436: 241–248.

    Article  CAS  Google Scholar 

  • Stevenson, R. J. & J. P. Smol, 2003. Use of algae in environmental assessments. In Wehr, J. D. & R. G. Sheath (eds), Freshwater Algae of North America Ecology and Classification. Academic Press, Amsterdam: 775–804.

    Chapter  Google Scholar 

  • ter Braak, C. & P. Šmilauer, 2002. CANOCO Reference Manual and CanoDraw for Windows User’s Guide-Software for Canonical Community Ordination (Version 4.5). Microcomputer Power, Ithaca, NY.

    Google Scholar 

  • Tian, Y., H. J. Liu, T. L. Zhang, K. K. Kwon, S. J. Kim & C. L. Yan, 2008. PAHs contamination and bacterial communities in mangrove surface sediments of the Jiulong River Estuary, China. Marine Pollution Bulletin 57: 707–715.

    Article  PubMed  CAS  Google Scholar 

  • Troussellier, M., H. Schafer, N. Batailler, L. Bernard, C. Courties, P. Lebaron, G. Muyzer, P. Servais & J. Vives-Rego, 2002. Bacterial activity and genetic richness along an estuarine gradient (Rhone River plume, France). Aquatic Microbial Ecology 28: 13–24.

    Article  Google Scholar 

  • Vartoukian, S. R., R. M. Palmer & W. G. Wade, 2010. Strategies for culture of unculturable bacteria. FEMS Microbiology Letters 309: 1–7.

    PubMed  CAS  Google Scholar 

  • Wang, W. P., H. S. Hong, L. P. Zhang, W. Z. Cao, Q. S. Jiang & J. L. Huang, 2005. Agricultural non-point source pollution information system of a mesoscale river watershed in southeast China. Environmental Informatics Archives 3: 58–66.

    Google Scholar 

  • Warnecke, F., R. Amann & J. Pernthaler, 2004. Actinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages. Environmental Microbiology 6: 242–253.

    Article  PubMed  CAS  Google Scholar 

  • Winter, C., T. Hein, G. Kavka, R. L. Mach & A. H. Farnleitner, 2007. Longitudinal changes in the bacterial community composition of the Danube River: a whole-river approach. Applied and Environmental Microbiology 73: 421–431.

    Article  PubMed  CAS  Google Scholar 

  • Wu, Q. L., A. Chatzinotas, J. J. Wang & J. Boenigk, 2009. Genetic diversity of eukaryotic plankton assemblages in eastern Tibetan lakes differing by their salinity and altitude. Microbial Ecology 58: 569–581.

    Article  PubMed  CAS  Google Scholar 

  • Yu, Y., Q. Yan & W. Feng, 2008. Spatiotemporal heterogeneity of plankton communities in Lake Donghu, China, as revealed by PCR-denaturing gradient gel electrophoresis and its relation to biotic and abiotic factors. FEMS Microbiology Ecology 63: 328–337.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Y. Y., C. X. Huang, J. Yang & N. Z. Jiao, 2011. Interactions between marine microorganisms and their phages. Chinese Science Bulletin 56: 1770–1777.

    Article  CAS  Google Scholar 

  • Zwart, G., B. C. Crump, M. P. K. Agterveld, F. Hagen & S. K. Han, 2002. Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquatic Microbial Ecology 28: 141–145.

    Article  Google Scholar 

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Acknowledgments

We thank Xian Zhang for field sampling, Bo Wei, Huining Zhang and Xin Yu for determining nutrient concentrations (nitrogen, phosphorus, and carbon), and Qing Li for providing Fig. 1. We also thank David M. Wilkinson, Guangjie Chen, Wenjing Zhang, and two anonymous reviewers for their constructive comments and suggestions. This research was supported by the Knowledge Innovation Program of the Chinese Academy of Sciences (Nos. KZCX2-YW-QN401 and KZCX2-YW-Q02-04), the Xiamen Project of Science and Technology for Distinguished Young Scholars (No. 3502Z20116006), the Key Science and Technology Project of Fujian Province, China (No. 2009Y0044), the National Natural Science Foundation of China (No. 41006087), and the China International Science and Technology Cooperation Program (No. 2009DFB90120).

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Correspondence to Jun Yang.

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Liu, L., Yang, J. & Zhang, Y. Genetic diversity patterns of microbial communities in a subtropical riverine ecosystem (Jiulong River, southeast China). Hydrobiologia 678, 113–125 (2011). https://doi.org/10.1007/s10750-011-0834-x

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