Skip to main content
SpringerLink
Log in

Quantifying the effects of geographical and environmental factors on distribution of stream bacterioplankton within nature reserves of Fujian, China

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Bacterioplankton are important components of freshwater ecosystems and play essential roles in ecological functions and processes; however, little is known about their geographical distribution and the factors influencing their ecology, especially in stream ecosystems. To examine how geographical and environmental factors affect the composition of bacterioplankton communities, we used denaturing gradient gel electrophoresis and clone sequencing to survey bacterioplankton communities in 31 samples of streamwater from seven nature reserves in Fujian province, southeast China. Our results revealed that dominant bacterioplankton communities exhibited a distinct geographical pattern. Further, we provided evidence for distance decay relationships in bacterioplankton community similarity and found similar community gradients in response to elevation and latitude. Both redundancy analyses and Mantel tests showed that bacterioplankton community composition was significantly correlated with both environmental (electrical conductivity, total phosphorus, and PO4-P) and geographical factors (latitude, longitude, and elevation). Variance partitioning further showed that the joint effect of geographical and environmental factors explained the largest proportion of the variation in distribution of bacterioplankton communities (13.6 %), followed by purely geographical factors (11.2 %), and purely environmental factors (0.6 %). The Betaproteobacteria were the most common taxa in the streams, followed by Firmicutes and Gammaproteobacteria. Therefore, our results suggest that the biogeographical patterns of stream bacterioplankton communities across the Fujian nature reserves are more influenced by geographical factors than by local physicochemical properties.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  Google Scholar 

  • Araya R, Tani K, Takagi T, Yamaguchi N, Nasu M (2003) Bacterial activity and community composition in stream water and biofilm from an urban river determined by fluorescent in situ hybridization and DGGE analysis. FEMS Microbiol Ecol 43:111–119

    Article  CAS  Google Scholar 

  • Astorga A, Oksanen J, Luoto M, Soininen J, Virtanen R, Muotka T (2012) Distance decay of similarity in freshwater communities: do macro- and microorganisms follow the same rules? Glob Ecol Biogeogr 21:365–375

    Article  Google Scholar 

  • Beier S, Witzel KP, Marxsen J (2008) Bacterial community composition in Central European running waters examined by temperature gradient gel electrophoresis and sequence analysis of 16S rRNA genes. Appl Environ Microbiol 74:188–199

    Article  CAS  Google Scholar 

  • Bianchi F, Acri F, Aubry FB, Berton A, Boldrin A, Camatti E, Cassin D, Comaschi A (2003) Can plankton communities be considered as bio-indicators of water quality in the Lagoon of Venice? Mar Pollut Bull 46:964–971

    Article  CAS  Google Scholar 

  • Clarke KR, Gorley RN (2001) PRIMER v5: User Manual/Tutorial. PRIMER-E, Plymouth, UK

    Google Scholar 

  • Crump BC, Adams HE, Hobbie JE, Kling GW (2007) Biogeography of bacterioplankton in lakes and streams of an arctic tundra catchment. Ecology 88:1365–1378

    Article  Google Scholar 

  • Dudgeon D (2014) Threats to freshwater biodiversity in a changing world. In: Freedman B (ed) Global Environmental Change. Springer Science + Business Media, Dordrecht, The Netherlands, pp 243–253

    Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631

    Article  CAS  Google Scholar 

  • Fierer N, McCain CM, Meir P, Zimmermann M, Rapp JM, Silman MR, Knight R (2011) Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92:797–804

    Article  Google Scholar 

  • Freimann R, Bürgmann H, Findlay SE, Robinson CT (2013) Bacterial structures and ecosystem functions in glaciated floodplains: contemporary states and potential future shifts. ISME J 7:2361–2373

    Article  CAS  Google Scholar 

  • Fuhrman JA (2009) Microbial community structure and its functional implications. Nature 459:193–199

    Article  CAS  Google Scholar 

  • Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL, Brown JH (2008) A latitudinal diversity gradient in planktonic marine bacteria. Proc Natl Acad Sci U S A 105:7774–7778

    Article  CAS  Google Scholar 

  • Goldenberg A, Dam H, Loon EE, Vonk JA, Der HG, Admiraal W (2014) Eutrophication decreases distance decay of similarity in diatom communities. Freshw Biol 59:1522–1531

    Article  Google Scholar 

  • Green J, Bohannan BJ (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evol 21:501–507

    Article  Google Scholar 

  • Hall T (1999) Biological sequence alignment editor for Win95/98/NT/2 K/XP. Ibis Biosciences, Carlsbad, CA, USA

    Google Scholar 

  • Hall RO, Meyer JL (1998) The trophic significance of bacteria in a detritus-based stream food web. Ecology 79:1995–2012

    Article  Google Scholar 

  • Hart DR, Stone L, Berman T (2000) Seasonal dynamics of the Lake Kinneret food web: the importance of the microbial loop. Limnol Oceanogr 45:350–361

    Article  CAS  Google Scholar 

  • Hu AY, Yang XY, Chen NW, Hou LY, Ma Y, Yu CP (2014) Response of bacterial communities to environmental changes in a mesoscale subtropical watershed, Southeast China. Sci Total Environ 472:746–756

    Article  CAS  Google Scholar 

  • Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton, NJ, USA

    Google Scholar 

  • Hullar MA, Kaplan LA, Stahl DA (2006) Recurring seasonal dynamics of microbial communities in stream habitats. Appl Environ Microbiol 72:713–722

    Article  CAS  Google Scholar 

  • Humbert JF, Dorigo U, Cecchi P, Berre BL, Debroas D, Bouvy M (2009) Comparison of the structure and composition of bacterial communities from temperate and tropical freshwater ecosystems. Environ Microbiol 11:2339–2350

    Article  CAS  Google Scholar 

  • Johnson RK, Angeler DG (2014) Effects of agricultural land use on stream assemblages: taxon-specific responses of alpha and beta diversity. Ecol Indic 45:386–393

    Article  CAS  Google Scholar 

  • Kingsford RT, Biggs HC, Pollard SR (2011) Strategic adaptive management in freshwater protected areas and their rivers. Biol Conserv 144:1194–1203

    Article  Google Scholar 

  • Ladau J, Sharpton TJ, Finucane MM, Jospin G, Kembel SW, O’Dwyer J, Koeppel AF, Green JL, Pollard KS (2013) Global marine bacterial diversity peaks at high latitudes in winter. ISME J 7:1669–1677

    Article  CAS  Google Scholar 

  • Langenheder S, Ragnarsson H (2007) The role of environmental and spatial factors for the composition of aquatic bacterial communities. Ecology 88:2154–2161

    Article  Google Scholar 

  • Lear G, Washington V, Neale M, Case B, Buckley H, Lewis G (2013) The biogeography of stream bacteria. Glob Ecol Biogeogr 22:544–554

    Article  Google Scholar 

  • Legendre P (2008) Studying beta diversity: ecological variation partitioning by multiple regression and canonical analysis. J Plant Ecol 1:3–8

    Article  Google Scholar 

  • Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge, UK

    Book  Google Scholar 

  • Liu LM, Yang J, Zhang YY (2011) Genetic diversity patterns of microbial communities in a subtropical riverine ecosystem (Jiulong River, southeast China). Hydrobiologia 678:113–125

    Article  CAS  Google Scholar 

  • Liu Z, Huang S, Sun G, Xu Z, Xu M (2012) Phylogenetic diversity, composition and distribution of bacterioplankton community in the Dongjiang River, China. FEMS Microbiol Ecol 80:30–44

    Article  CAS  Google Scholar 

  • Liu LM, Yang J, Yu XQ, Chen GJ, Yu Z (2013) Patterns in the composition of microbial communities from a subtropical river: effects of environmental, spatial and temporal factors. PLoS One 8:e81232

    Article  Google Scholar 

  • Liu LM, Yang J, Yu Z, Wilkinson DM (2015) The biogeography of abundant and rare bacterioplankton in lakes and reservoirs of China. ISME J. doi:10.1038/ismej.2015.29

  • Lovejoy TE (2006) Protected areas: a prism for a changing world. Trends Ecol Evol 21:329–333

    Article  Google Scholar 

  • Martinuzzi S, Januchowski-Hartley SR, Pracheil BM, McIntyre PB, Plantinga AJ, Lewis DJ, Radeloff VC (2014) Threats and opportunities for freshwater conservation under future land use change scenarios in the United States. Glob Chang Biol 20:113–124

    Article  Google Scholar 

  • Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreas L, Reysenbach A-L, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112

    Article  CAS  Google Scholar 

  • McCain CM (2009) Global analysis of bird elevational diversity. Glob Ecol Biogeogr 18:346–360

    Article  Google Scholar 

  • Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  Google Scholar 

  • Nekola JC, White PS (1999) The distance decay of similarity in biogeography and ecology. J Biogeogr 26:867–878

    Article  Google Scholar 

  • Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol R 75:14–49

    Article  CAS  Google Scholar 

  • Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87:2614–2625

    Article  Google Scholar 

  • Ponnusamy L, Xu N, Stav G, Wesson DM, Schal C, Apperson CS (2008) Diversity of bacterial communities in container habitats of mosquitoes. Microb Ecol 56:593–603

    Article  Google Scholar 

  • Portillo MC, Anderson SP, Fierer N (2012) Temporal variability in the diversity and composition of stream bacterioplankton communities. Environ Microbiol 14:2417–2428

    Article  Google Scholar 

  • Read DS, Gweon HS, Bowes MJ, Newbold LK, Field D, Bailey MJ, Griffiths RI (2015) Catchment-scale biogeography of riverine bacterioplankton. ISME J 9:516–526

    Article  CAS  Google Scholar 

  • Saunders DL, Meeuwig JJ, Vincent ACJ (2002) Freshwater protected areas: strategies for conservation. Conserv Biol 16:30–41

    Article  Google Scholar 

  • Schäfer H, Muyzer G (2001) Denaturing gradient gel electrophoresis in marine microbial ecology. Method Microbiol 30:425–468

    Article  Google Scholar 

  • Schiaffino MR, Unrein F, Gasol JM, Massana R, Balague V, Izaguirre I (2011) Bacterial community structure in a latitudinal gradient of lakes: the roles of spatial versus environmental factors. Freshw Biol 56:1973–1991

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Singh D, Shi LL, Adams JM (2013) Bacterial diversity in the mountains of South-West China: climate dominates over soil parameters. J Microbiol 51:439–447

    Article  CAS  Google Scholar 

  • Stomp M, Huisman J, Mittelbach GG, Litchman E, Klausmeier CA (2011) Large-scale biodiversity patterns in freshwater phytoplankton. Ecology 92:2096–2107

    Article  Google Scholar 

  • Suski CD, Cooke SJ (2007) Conservation of aquatic resources through the use of freshwater protected areas: opportunities and challenges. Biodivers Conserv 16:2015–2029

    Article  Google Scholar 

  • Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton, NJ, USA

    Google Scholar 

  • Tuomisto H, Ruokolainen K (2006) Analyzing or explaining beta diversity? understanding the targets of different methods of analysis. Ecology 87:2697–2708

    Article  Google Scholar 

  • Vallaeys T, Topp E, Muyzer G, Macheret V, Laguerre G, Rigaud A, Soulas G (1997) Evaluation of denaturing gradient gel electrophoresis in the detection of 16S rDNA sequence variation in rhizobia and methanotrophs. FEMS Microbiol Ecol 24:279–285

    Article  CAS  Google Scholar 

  • Virtanen L, Soininen J (2012) The roles of environment and space in shaping stream diatom communities. Eur J Phycol 47:160–168

    Article  Google Scholar 

  • Vörösmarty CJ, McIntyre PB, Gessner MO, Dudgeon D, Prusevich A, Green P, Glidden S, Bunn SE, Sullivan CA, Liermann CR, Davies PM (2010) Global threats to human water security and river biodiversity. Nature 467:555–561

    Article  Google Scholar 

  • Wang J, Shen J, Wu Y, Tu C, Soininen J, Stegen JC, He J, Liu X, Zhang L, Zhang E (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME J 7:1310–1321

    Article  CAS  Google Scholar 

  • Washington VJ, Lear G, Neale MW, Lewis GD (2013) Environmental effects on biofilm bacterial communities: a comparison of natural and anthropogenic factors in New Zealand streams. Freshw Biol 58:2277–2286

    Google Scholar 

  • Xu MY, Wu WM, Wu LY, He ZL, Van Nostrand JD, Deng Y, Luo J, Carley J, Ginder-Vogel M, Gentry TJ, Gu BH, Watson D, Jardine PM, Marsh TL, Tiedje JM, Hazen T, Criddle CS, Zhou JZ (2010) Responses of microbial community functional structures to pilot-scale uranium in situ bioremediation. ISME J 4:1060–1070

    Article  Google Scholar 

  • Yang J, Yu XQ, Liu LM, Zhang WJ, Guo PY (2012) Algae community and trophic state of subtropical reservoirs in southeast Fujian, China. Environ Sci Pollut Res 19:1432–1442

    Article  CAS  Google Scholar 

  • Zwart G, Crump BC, Kamst-van Agterveld MP, Hagen F, Han SK (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28:141–155

    Article  Google Scholar 

Download references

Acknowledgments

We thank Dr. Hongqu Tang for assistance in field sampling, and Mr. Huihuang Chen and Ms. Xiaoqing Yu for support in nutrient analysis. This study was financed by the International Science and Technology Cooperation Program of China (2011DFB91710), the Natural Science Foundation for Distinguished Young Scholars of Fujian Province (2012 J06009), and the National Natural Science Foundation of China (31370471 and U1133601). We thank Dr. David M. Wilkinson and our two referees for insightful comments which help improve the clarity of this paper.

Compliance with ethical standards

The authors have declared that no competing interests exist. No specific permissions were required for these activities. Informed consent was obtained from all participants and this field study did not involve endangered or protected species.

Author information

Authors and Affiliations

  1. Aquatic EcoHealth Group, Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Xiamen, 361021, China

    Yongming Wang, Jun Yang, Lemian Liu & Zheng Yu

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Yongming Wang

Authors
  1. Yongming Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lemian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zheng Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jun Yang.

Additional information

Responsible editor: Philippe Garrigues

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 3479 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Y., Yang, J., Liu, L. et al. Quantifying the effects of geographical and environmental factors on distribution of stream bacterioplankton within nature reserves of Fujian, China. Environ Sci Pollut Res 22, 11010–11021 (2015). https://doi.org/10.1007/s11356-015-4308-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4308-y

Keywords

Search

Navigation