Skip to main content
SpringerLink
Log in

Biogeography and Diversity of Freshwater Bacteria on a River Catchment Scale

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

To illustrate how freshwater bacterial community changes with geographic gradient, we investigated the spatial changes of bacterial abundance and community structures from over 200 samples on a catchment scale in the Songhua River using heterotrophic plate counts, flow cytometry, denaturing gradient gel electrophoresis, and pyrosequencing analysis. The results showed that the mainstream had higher cultivable bacteria and total bacterial concentration than tributaries in the Songhua River catchment. Response model analysis demonstrated that the bacterial community exhibits a biogeographical signature even in an interconnected river network system, and the total bacterial concentration and biodiversity were significantly correlated to latitude (p < 0.001) and longitude (p < 0.001). Multivariate redundancy analysis indicated that temperature was the most important factor driving bacterial community structure in the Songhua River, which accounts for 35.30% variance of communities, then dissolved oxygen (17.60%), latitude (17.60%), longitude (11.80%), and pH (5.88%). High-throughput pyrosequencing revealed that at the phylum level, Proteobacteria was numerically dominant (89.6%) in river catchment, followed by Bacteroidetes (8.1%) and Cyanobacteria (1.2%). The overall results revealed that the bacterial community was driven by geographical distance regardless of the continuum of the river on a catchment scale.

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
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506. https://doi.org/10.1038/nrmicro2795

    Article  CAS  PubMed  Google Scholar 

  2. Galand PE, Casamayor EO, Kirchman DL, Lovejoy C (2009) Ecology of the rare microbial biosphere of the Arctic Ocean. Proc Natl Acad Sci U S A 106:22427–22432. https://doi.org/10.1073/pnas.0908284106

    Article  PubMed  PubMed Central  Google Scholar 

  3. Livermore JA, Jones SE (2015) Local-global overlap in diversity informs mechanisms of bacterial biogeography. ISME J 9:2413–2422. https://doi.org/10.1038/ismej.2015.51

    Article  PubMed  PubMed Central  Google Scholar 

  4. Liu L, Yang J, Yu Z, Wilkinson DM (2015) The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China. ISME J 9:2068–2077. https://doi.org/10.1038/ismej.2015.29

    Article  PubMed  PubMed Central  Google Scholar 

  5. Soininen J, Korhonen JJ, Luoto M (2013) Stochastic species distributions are driven by organism size. Ecology 94:660–670

    Article  PubMed  Google Scholar 

  6. Stacy A, McNally L, Darch SE, Brown SP, Whiteley M (2016) The biogeography of polymicrobial infection. Nat Rev Microbiol 14:93–105. https://doi.org/10.1038/nrmicro.2015.8

    Article  CAS  PubMed  Google Scholar 

  7. Bowen JL, Crump BC, Deegan LA, Hobbie JE (2009) Salt marsh sediment bacteria: their distribution and response to external nutrient inputs. ISME J 3:924–934. https://doi.org/10.1038/ismej.2009.44

    Article  CAS  PubMed  Google Scholar 

  8. Tiquia SM (2010) Metabolic diversity of the heterotrophic microorganisms and potential link to pollution of the Rouge River. Environ Pollut 158:1435–1443. https://doi.org/10.1016/j.envpol.2009.12.035

    Article  CAS  PubMed  Google Scholar 

  9. 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. https://doi.org/10.1038/ismej.2013.30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Van der Gucht K, Cottenie K, Muylaert K, Vloemans N, Cousin S, Declerck S, Jeppesen E, Conde-Porcuna J-M, Schwenk K, Zwart G, Degans H, Vyverman W, De Meester L (2007) The power of species sorting: local factors drive bacterial community composition over a wide range of spatial scales. Proc Natl Acad Sci U S A 104:20404–20409. https://doi.org/10.1073/pnas.0707200104

    Article  PubMed  PubMed Central  Google Scholar 

  11. Winter C, Matthews B, Suttle CA (2013) Effects of environmental variation and spatial distance on Bacteria, archaea and viruses in sub-polar and arctic waters. ISME J 7:1507–1518. https://doi.org/10.1038/ismej.2013.56

    Article  PubMed  PubMed Central  Google Scholar 

  12. Oakley BB, Carbonero F, van der Gast CJ, Hawkins RJ, Purdy KJ (2010) Evolutionary divergence and biogeography of sympatric niche-differentiated bacterial populations. ISME J 4:488–497. https://doi.org/10.1038/ismej.2009.146

    Article  PubMed  Google Scholar 

  13. Martiny JBH, Eisen JA, Penn K, Allison SD, Horner-Devine MC (2011) Drivers of bacterial beta-diversity depend on spatial scale. Proc Natl Acad Sci U S A 108:7850–7854. https://doi.org/10.1073/pnas.1016308108

    Article  PubMed  PubMed Central  Google Scholar 

  14. Liu J, Wang J, Gao G, Bartlam MG, Wang Y (2015) Distribution and diversity of fungi in freshwater sediments on a river catchment scale. Front Microbiol 6:329. https://doi.org/10.3389/fmicb.2015.00329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Fuhrman JA (2009) Microbial community structure and its functional implications. Nature 459:193–199. https://doi.org/10.1038/nature08058

    Article  CAS  PubMed  Google Scholar 

  16. Pagaling E, Strathdee F, Spears BM, Cates ME, Allen RJ, Free A (2014) Community history affects the predictability of microbial ecosystem development. ISME J 8:19–30. https://doi.org/10.1038/ismej.2013.150

    Article  PubMed  Google Scholar 

  17. Barton AD, Dutkiewicz S, Flierl G, Bragg J, Follows MJ (2010) Patterns of diversity in marine phytoplankton. Science 327:1509–1511. https://doi.org/10.1126/science.1184961

    Article  CAS  PubMed  Google Scholar 

  18. Bissett A, Richardson AE, Baker G, Wakelin S, Thrall PH (2010) Life history determines biogeographical patterns of soil bacterial communities over multiple spatial scales. Mol Ecol 19:4315–4327. https://doi.org/10.1111/j.1365-294X.2010.04804.x

    Article  CAS  PubMed  Google Scholar 

  19. 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. https://doi.org/10.1038/ismej.2014.166

    Article  CAS  PubMed  Google Scholar 

  20. Savio D, Sinclair L, Ijaz UZ, Parajka J, Reischer GH, Stadler P, Blaschke AP, Bloeschl G, Mach RL, Kirschner AKT, Farnleitner AH, Eiler A (2015) Bacterial diversity along a 2600 km river continuum. Environ Microbiol 17:4994–5007. https://doi.org/10.1111/1462-2920.12886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hu A, Yang X, Chen N, Hou L, Ma Y, Yu C-P (2014) Response of bacterial communities to environmental changes in a mesoscale subtropical watershed, Southeast China. Sci Total Environ 472:746–756. https://doi.org/10.1016/j.scitotenv.2013.11.097

    Article  CAS  PubMed  Google Scholar 

  22. Wang SJ, Wang YJ, Ran LS, Su T (2015) Climatic and anthropogenic impacts on runoff changes in the Songhua River basin over the last 56 years (1955-2010), Northeastern China. Catena 127:258–269. https://doi.org/10.1016/j.catena.2015.01.004

    Article  Google Scholar 

  23. Boon N, De Windt W, Verstraete W, Top EM (2002) Evaluation of nested PCR-DGGE (denaturing gradient gel electrophoresis) with group-specific 16S rRNA primers for the analysis of bacterial communities from different wastewater treatment plants. FEMS Microbiol Ecol 39:101–112. https://doi.org/10.1016/s0168-6496(01)00198-2

    Article  CAS  PubMed  Google Scholar 

  24. Ma L, Mao G, Liu J, Gao G, Zou C, Bartlam MG, Wang Y (2016) Spatial-temporal changes of bacterioplankton community along an exhorheic river. Front Microbiol 7:250. https://doi.org/10.3389/fmicb.2016.00250

  25. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063. https://doi.org/10.1126/science.1070710

    Article  CAS  PubMed  Google Scholar 

  28. Karrasch B, Mehrens M, Rosenlöcher Y, Peters K (2001) The dynamics of phytoplankton, bacteria and heterotrophic flagellates at two banks near Magdeburg in the river Elbe (Germany). Limnologica 31:93–107. https://doi.org/10.1016/S0075-9511(01)80002-5

    Article  Google Scholar 

  29. Berger B, Hoch B, Kavka G, Herndl GJ (1996) Bacterial colonization of suspended solids in the river Danube. Aquat Microb Ecol 10:37–44. https://doi.org/10.3354/ame010037

    Article  Google Scholar 

  30. Bergfeld T, Scherwass A, Ackermann B, Fischer H, Arndt H, Schoel A (2011) Longitudinal and seasonal dynamics of the planktonic microbial community along the length of the river Rhine. River Syst 19:337–349. https://doi.org/10.1127/1868-5749/2011/0037

    Article  Google Scholar 

  31. Troussellier M, Got P, Bouvy M, Mboup M, Arfi R, Lebihan F, Monfort P, Corbin D, Bernard C (2004) Water quality and health status of the Senegal River estuary. Mar Pollut Bull 48:852–862. https://doi.org/10.1016/j.marpolbul.2003.10.028

    Article  CAS  PubMed  Google Scholar 

  32. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631. https://doi.org/10.1073/pnas.0507535103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Chen J, Wang P, Wang C, Wang X, Miao L, Liu S, Yuan Q (2018) Bacterial communities in riparian sediments: a large-scale longitudinal distribution pattern and response to dam construction. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.00999

  34. Liu T, Zhang AN, Wang J, Liu S, Jiang X, Dang C, Ma T, Liu S, Chen Q, Xie S, Zhang T, Ni J (2018) Integrated biogeography of planktonic and sedimentary bacterial communities in the Yangtze River. Microbiome 6:16. https://doi.org/10.1186/s40168-017-0388-x

    Article  PubMed  PubMed Central  Google Scholar 

  35. Sul WJ, Oliver TA, Ducklow HW, Amaral-Zettler LA, Sogin ML (2013) Marine bacteria exhibit a bipolar distribution. Proc Natl Acad Sci U S A 110:2342–2347. https://doi.org/10.1073/pnas.1212424110

    Article  PubMed  PubMed Central  Google Scholar 

  36. Rouquette JR, Dallimer M, Armsworth PR, Gaston KJ, Maltby L, Warren PH (2013) Species turnover and geographic distance in an urban river network. Divers Distrib 19:1429–1439. https://doi.org/10.1111/ddi.12120

    Article  Google Scholar 

  37. Shiah FK, Ducklow HW (1994) Temperature and substrate regulation of bacterial abundance, production and specific growth rate in Chesapeake Bay, USA. Mar Ecol Prog Ser 103:297–308

    Article  Google Scholar 

  38. Zaitseva SV, Abidueva EY, Buryukhaev SP, Namsaraev BB (2012) Factors controlling the activity of the microbial community of the alkaline Lake Beloe (Transbaikal region). Microbiology 81:468–476. https://doi.org/10.1134/s0026261712040170

    Article  CAS  Google Scholar 

  39. Volant A, Bruneel O, Desoeuvre A, Hery M, Casiot C, Bru N, Delpoux S, Fahy A, Javerliat F, Bouchez O, Duran R, Bertin PN, Elbaz-Poulichet F, Lauga B (2014) Diversity and spatiotemporal dynamics of bacterial communities: physicochemical and other drivers along an acid mine drainage. FEMS Microbiol Ecol 90:247–263. https://doi.org/10.1111/1574-6941.12394

    Article  CAS  PubMed  Google Scholar 

  40. Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci U S A 106:12788–12793. https://doi.org/10.1073/pnas.0902080106

    Article  PubMed  PubMed Central  Google Scholar 

  41. Wilhelm L, Singer GA, Fasching C, Battin TJ, Besemer K (2013) Microbial biodiversity in glacier-fed streams. ISME J 7:1651–1660. https://doi.org/10.1038/ismej.2013.44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Boeer SI, Hedtkamp SIC, van Beusekom JEE, Fuhrman JA, Boetius A, Ramette A (2009) Time- and sediment depth-related variations in bacterial diversity and community structure in subtidal sands. ISME J 3:780–791. https://doi.org/10.1038/ismej.2009.29

    Article  CAS  Google Scholar 

  43. Nemergut DR, Costello EK, Hamady M, Lozupone C, Jiang L, Schmidt SK, Fierer N, Townsend AR, Cleveland CC, Stanish L, Knight R (2011) Global patterns in the biogeography of bacterial taxa. Environ Microbiol 13:135–144. https://doi.org/10.1111/j.1462-2920.2010.02315.x

    Article  PubMed  PubMed Central  Google Scholar 

  44. 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. https://doi.org/10.1111/j.1574-6941.2011.01268.x

    Article  CAS  PubMed  Google Scholar 

  45. Sekiguchi H, Watanabe M, Nakahara T, Xu BH, 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. https://doi.org/10.1128/aem.68.10.5142-5150.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Lyautey E, Jackson CR, Cayrou J, Rols JL, Garabetian F (2005) Bacterial community succession in natural river biofilm assemblages. Microb Ecol 50:589–601. https://doi.org/10.1007/s00248-005-5032-9

    Article  PubMed  Google Scholar 

  47. Wang P, Wang X, Wang C, Miao L, Hou J, Yuan Q (2017) Shift in bacterioplankton diversity and structure: influence of anthropogenic disturbances along the Yarlung Tsangpo River on the Tibetan Plateau, China. Sci Rep 7:12529. https://doi.org/10.1038/s41598-017-12893-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Arandia-Gorostidi N, Huete-Stauffer TM, Alonso-Saez L, Moran XAG (2017) Testing the metabolic theory of ecology with marine bacteria: different temperature sensitivity of major phylogenetic groups during the spring phytoplankton bloom. Environ Microbiol 19:4493–4505. https://doi.org/10.1111/1462-2920.13898

    Article  CAS  PubMed  Google Scholar 

  49. Palomo A, Fowler SJ, Gulay A, Rasmussen S, Sicheritz-Ponten T, Smets BF (2016) Metagenomic analysis of rapid gravity sand filter microbial communities suggests novel physiology of Nitrospira spp. ISME J 10:2569–2581. https://doi.org/10.1038/ismej.2016.63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Ferrera I, Aristegui J, Gonzalez JM, Montero MF, Fraile-Nuez E, Gasol JM (2015) Transient changes in bacterioplankton communities induced by the submarine volcanic eruption of El Hierro (Canary Islands). PLoS One 10:e0118136. https://doi.org/10.1371/journal.pone.0118136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Zhou J, Song X, Zhang C-Y, Chen G-F, Lao Y-M, Jin H, Cai Z-H (2018) Distribution patterns of microbial community structure along a 7000-mile latitudinal transect from the Mediterranean Sea across the Atlantic Ocean to the Brazilian Coastal Sea. Microb Ecol 76:592–609. https://doi.org/10.1007/s00248-018-1150-z

    Article  CAS  PubMed  Google Scholar 

  52. Ju F, Zhang T (2015) Bacterial assembly and temporal dynamics in activated sludge of a full-scale municipal wastewater treatment plant. ISME J 9:683–695. https://doi.org/10.1038/ismej.2014.162

    Article  CAS  PubMed  Google Scholar 

  53. Ruiz-Gonzalez C, Proia L, Ferrera I, Gasol JM, Sabater S (2013) Effects of large river dam regulation on bacterioplankton community structure. FEMS Microbiol Ecol 84:316–331. https://doi.org/10.1111/1574-6941.12063

    Article  CAS  PubMed  Google Scholar 

  54. Ibekwe AM, Ma JC, Murinda SE (2016) Bacterial community composition and structure in an Urban River impacted by different pollutant sources. Sci Total Environ 566:1176–1185. https://doi.org/10.1016/j.scitotenv.2016.05.168

    Article  CAS  PubMed  Google Scholar 

  55. Wey JK, Juergens K, Weitere M (2012) Seasonal and successional influences on bacterial community composition exceed that of protozoan grazing in river biofilms. Appl Environ Microbiol 78:2013–2024. https://doi.org/10.1128/aem.06517-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Grossart HP, Ploug H (2000) Bacterial production and growth efficiencies: direct measurements on riverine aggregates. Limnol Oceanogr 45(2):436–445. https://doi.org/10.4319/lo.2000.45.2.0436

    Article  CAS  Google Scholar 

  57. Gilbert JA, Steele JA, Caporaso JG, Steinbrueck L, Reeder J, Temperton B, Huse S, McHardy AC, Knight R, Joint I, Somerfield P, Fuhrman JA, Field D (2012) Defining seasonal marine microbial community dynamics. ISME J 6:298–308. https://doi.org/10.1038/ismej.2011.107

    Article  CAS  PubMed  Google Scholar 

  58. Zwirglmaier K, Keiz K, Engel M, Geist J, Raeder U (2015) Seasonal and spatial patterns of microbial diversity along a trophic gradient in the interconnected lakes of the Osterseen Lake District, Bavaria. Front Microbiol 6:1168. https://doi.org/10.3389/fmicb.2015.01168

    Article  PubMed  PubMed Central  Google Scholar 

  59. Liu J, Hao Z, Ma L, Ji Y, Bartlam M, Wang Y (2016) Spatio-temporal variations of high and low nucleic acid content bacteria in an exorheic river. PLoS One 11:e0153678. https://doi.org/10.1371/journal.pone.0153678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by National Key Basic Research Development Program [grant number 2015CB459000], Chinese National Science Foundation [grant numbers 31670498 and 31322012], China Postdoctoral Science Foundation [grant number 2016M591190], and the Fundamental Research Funds for the Central Universities. We thank Prof. Zhou Qixing and Dr. Sun Xiaoyin for their kind help in sampling and physico-chemical analysis of the water samples.

Author information

Authors and Affiliations

  1. Key Laboratory of Pollution Processes and Environmental Criteria (Ministry of Education), College of Environmental Science and Engineering, Nankai University, Tianjin, 300350, China

    Jie Liu, Teng Tu, Guanghai Gao & Yingying Wang

  2. Graduate School at Shenzhen, Tsinghua University, Shenzhen, 518055, China

    Jie Liu

  3. Center for Earth Environment and Resources, Sun Yat-Sen University, Guangzhou, 510275, China

    Teng Tu

  4. State Key Laboratory of Medicinal Chemical Biology & College of Life Sciences, Nankai University, Tianjin, 300071, China

    Mark Bartlam

Authors
  1. Jie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Teng Tu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guanghai Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mark Bartlam
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yingying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yingying Wang.

Electronic Supplementary Material

ESM 1

(DOCX 231 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, J., Tu, T., Gao, G. et al. Biogeography and Diversity of Freshwater Bacteria on a River Catchment Scale. Microb Ecol 78, 324–335 (2019). https://doi.org/10.1007/s00248-019-01323-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-019-01323-9

Keywords

Search

Navigation