Coordinated Metacommunity Assembly and Spatial Distribution of Multiple Microbial Kingdoms within a Lake

  • So-Yeon Jeong
  • Jong-Yun Choi
  • Tae Gwan KimEmail author
Microbiology of Aquatic Systems


Freshwater planktonic communities comprise a tremendous diversity of microorganisms. This study investigated the distribution patterns of microbial kingdoms (bacteria, fungi, protists, and microbial metazoans) within a lake ecosystem. Water samples were collected from 50 sites along the shoreline in a lake during an early eutrophication period, and MiSeq sequencing was performed with different marker genes. Metacommunity analyses revealed a bimodal occupancy-frequency distribution and a Clementsian gradient persisting throughout all microbial kingdoms, suggesting similar regional processes in all kingdoms. Variation partitioning revealed that environmental characteristics, macrophyte/macroinvertebrate composition, space coordinates, and distance-based Moran’s eigenvector maps (dbMEM) together could explain up to 29% of the community variances in microbial kingdoms. Kingdom synchrony results showed strong couplings between kingdoms (R2 ≥ 0.31), except between Fungi and Metazoa (R2 = 0.09). Another variation partitioning revealed that microbial kingdoms could well explain their community variances up to 73%. Interestingly, the kingdom Protista was best synchronized with the other kingdoms. A correlation network showed that positive associations between kingdoms outnumbered the negative ones and that the kingdom Protista acted as a hub among kingdoms. Module analysis showed that network modules included multi-kingdom associations that were prevalent. Our findings suggest that protists coordinate community assembly and distribution of other kingdoms, and inter-kingdom interactions are a key determinant in shaping their community structures in a freshwater lake.


Planktonic community Spatial dynamics Microbial kingdoms Freshwater lake Microbial network 


Funding Information

This study was supported by the basic science research program through the National Research Foundation of Korea funded by the Ministry of Education (2018R1D1A1B07048872).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2019_1453_MOESM1_ESM.pdf (1.6 mb)
ESM 1 (PDF 1636 kb)


  1. 1.
    Šimek K, Jürgens K, Nedoma J, Comerma M, Armengol J (2000) Ecological role and bacterial grazing of Halteria spp.: small freshwater oligotrichs as dominant pelagic ciliate bacterivores. Aquat Microb Ecol 22:43–56CrossRefGoogle Scholar
  2. 2.
    Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Hättenschwiler S (2010) Diversity meets decomposition. Trends Ecol Evol 25:372–380. CrossRefPubMedGoogle Scholar
  3. 3.
    Cotner JB, Biddanda BA (2002) Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5:105–121. CrossRefGoogle Scholar
  4. 4.
    Fuhrman JA (2009) Microbial community structure and its functional implications. Nature 459:193–199. CrossRefPubMedGoogle Scholar
  5. 5.
    Comte J, Jacquet S, Viboud S, Fontvieille D, Millery A, Paolini G, Domaizon I (2006) Microbial community structure and dynamics in the largest natural French lake (Lake Bourget). Microb Ecol 52:72–89. CrossRefPubMedGoogle Scholar
  6. 6.
    Debroas D, Domaizon I, Humbert J-F, Jardillier L, Lepère C, Oudart A, Taïb N (2017) Overview of freshwater microbial eukaryotes diversity: a first analysis of publicly available metabarcoding data. FEMS Microbiol Ecol 93:1–14. CrossRefGoogle Scholar
  7. 7.
    Henriques-Silva R, Lindo Z, Peres-Neto PR (2013) A community of metacommunities: exploring patterns in species distributions across large geographical areas. Ecology 94:627–639. CrossRefPubMedGoogle Scholar
  8. 8.
    Langenheder S, Wang J, Karjalainen SM, Laamanen TM, Tolonen KT, Vilmi A, Heino J (2017) Bacterial metacommunity organization in a highly connected aquatic system. FEMS Microbiol Ecol 93:1–9. CrossRefGoogle Scholar
  9. 9.
    Presley SJ, Higgins CL, Willig MR (2010) A comprehensive framework for the evaluation of metacommunity structure. Oikos 119:908–917. CrossRefGoogle Scholar
  10. 10.
    Gilbert JA, Steele JA, Caporaso JG, Steinbrück L, Reeder J, Temperton B, Huse S, McHardy AC, Knight R, Joint I (2012) Defining seasonal marine microbial community dynamics. ISME J 6:298–308. CrossRefPubMedGoogle Scholar
  11. 11.
    Caron DA, Worden AZ, Countway PD, Demir E, Heidelberg KB (2008) Protists are microbes too: a perspective. ISME J 3:4–12. CrossRefPubMedGoogle Scholar
  12. 12.
    Grossart H-P, Rojas-Jimenez K (2016) Aquatic fungi: targeting the forgotten in microbial ecology. Curr Opin Microbiol 31:140–145. CrossRefPubMedGoogle Scholar
  13. 13.
    Adrian R, Wickham SA, Butler NM (2001) Trophic interactions between zooplankton and the microbial community in contrasting food webs: the epilimnion and deep chlorophyll maximum of a mesotrophic lake. Aquat Microb Ecol 24:83–97CrossRefGoogle Scholar
  14. 14.
    Wickham SA (1995) Trophic relations between cyclopoid copepods and ciliated protists: complex interactions link the microbial and classic food webs. Limnol Oceanogr 40:1173–1181CrossRefGoogle Scholar
  15. 15.
    Torstensson A, Dinasquet J, Chierici M, Fransson A, Riemann L, Wulff A (2015) Physicochemical control of bacterial and protist community composition and diversity in Antarctic sea ice. Environ Microbiol 17:3869–3881. CrossRefPubMedGoogle Scholar
  16. 16.
    Montagna M, Berruti A, Bianciotto V, Cremonesi P, Giannico R, Gusmeroli F, Lumini E, Pierce S, Pizzi F, Turri F (2018) Differential biodiversity responses between kingdoms (plants, fungi, bacteria and metazoa) along an Alpine succession gradient. Mol Ecol 27:3671–3685. CrossRefPubMedGoogle Scholar
  17. 17.
    Lepère C, Domaizon I, Taïb N, Mangot J-F, Bronner G, Boucher D, Debroas D (2013) Geographic distance and ecosystem size determine the distribution of smallest protists in lacustrine ecosystems. FEMS Microbiol Ecol 85:85–94. CrossRefPubMedGoogle Scholar
  18. 18.
    Liu L, Yang J, Yu X, Chen G, Yu Z (2013) Patterns in the composition of microbial communities from a subtropical river: effects of environmental, spatial and temporal factors. PLoS One 8:1–10. CrossRefGoogle Scholar
  19. 19.
    Zhang H, Huang X, Huang L, Bao F, Xiong S, Wang K, Zhang D (2018) Microeukaryotic biogeography in the typical subtropical coastal waters with multiple environmental gradients. Sci Total Environ 635:618–628. CrossRefPubMedGoogle Scholar
  20. 20.
    Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl Environ Microbiol 71:227–239. CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Muylaert K, Van der Gucht K, Vloemans N, De Meester L, Gillis M, Vyverman W (2002) Relationship between bacterial community composition and bottom-up versus top-down variables in four eutrophic shallow lakes. Appl Environ Microbiol 68:4740–4750. CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Bock C, Salcher M, Jensen M, Pandey RV, Boenigk J (2018) Synchrony of eukaryotic and prokaryotic planktonic communities in three seasonally sampled Austrian lakes. Front Microbiol 9:1290. CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Aguilar P, Dorador C, Vila I, Sommaruga R (2018) Bacterioplankton composition in tropical high-elevation lakes of the Andean plateau. FEMS Microbiol Ecol 94:1–9. CrossRefGoogle Scholar
  24. 24.
    Choi J-Y, Jeong K-S, Kim S-K, La G-H, Chang K-H, Joo G-J (2014) Role of macrophytes as microhabitats for zooplankton community in lentic freshwater ecosystems of South Korea. Ecol Inform 24:177–185. CrossRefGoogle Scholar
  25. 25.
    Wetzel RG, Likens GE (2000) Limnolgical analyses. Springer, New YorkCrossRefGoogle Scholar
  26. 26.
    APHA (1992) Standard methods for the examination of water and wastewater. American Public Health Association, Washington, DCGoogle Scholar
  27. 27.
    Kim TG, Moon K-E, Yun J, Cho K-S (2013) Comparison of RNA- and DNA-based bacterial communities in a lab-scale methane-degrading biocover. Appl Microbiol Biotechnol 97:3171–3181. CrossRefPubMedGoogle Scholar
  28. 28.
    Mueller RC, Gallegos-Graves LV, Kuske CR (2016) A new fungal large subunit ribosomal RNA primer for high-throughput sequencing surveys. FEMS Microbiol Ecol 92:1–11. CrossRefGoogle Scholar
  29. 29.
    Hugerth LW, Muller EE, Hu YO, Lebrun LA, Roume H, Lundin D, Wilmes P, Andersson AF (2014) Systematic design of 18S rRNA gene primers for determining eukaryotic diversity in microbial consortia. PLoS One 9:1–11. CrossRefGoogle Scholar
  30. 30.
    Székely AJ, Langenheder S (2014) The importance of species sorting differs between habitat generalists and specialists in bacterial communities. FEMS Microbiol Ecol 87:102–112. CrossRefPubMedGoogle Scholar
  31. 31.
    Dallas T (2014) metacom: an R package for the analysis of metacommunity structure. Ecography 37:402–405. CrossRefGoogle Scholar
  32. 32.
    Mehranvar L, Jackson DA (2001) History and taxonomy: their roles in the core-satellite hypothesis. Oecologia 127:131–142. CrossRefPubMedGoogle Scholar
  33. 33.
    Lindh MV, Sjöstedt J, Ekstam B, Casini M, Lundin D, Hugerth LW, Hu YOO, Andersson AF, Andersson A, Legrand C, Pinhassi J (2017) Metapopulation theory identifies biogeographical patterns among core and satellite marine bacteria scaling from tens to thousands of kilometers. Environ Microbiol 19:1222–1236. CrossRefPubMedGoogle Scholar
  34. 34.
    Hanski I (1982) Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38:210–221. CrossRefGoogle Scholar
  35. 35.
    Hanski I, Gyllenberg M (1993) Two general metapopulation models and the core-satellite species hypothesis. Am Nat 142:17–41CrossRefGoogle Scholar
  36. 36.
    Freckleton RP, Gill JA, Noble D, Watkinson AR (2005) Large-scale population dynamics, abundance–occupancy relationships and the scaling from local to regional population size. J Anim Ecol 74:353–364. CrossRefGoogle Scholar
  37. 37.
    Wurzbacher CM, Bärlocher F, Grossart HP (2010) Fungi in lake ecosystems. Aquat Microb Ecol 59:125–149. CrossRefGoogle Scholar
  38. 38.
    Yeh YC, Peres-Neto PR, Huang SW, Lai YC, Tu CY, Shiah FK, Gong GC, Hsieh C (2015) Determinism of bacterial metacommunity dynamics in the southern East China Sea varies depending on hydrography. Ecography 38:198–212. CrossRefGoogle Scholar
  39. 39.
    Zeng J, Bian Y, Xing P, Wu QL (2012) Macrophyte species drive the variation of bacterioplankton community composition in a shallow freshwater lake. Appl Environ Microbiol 78:177–184. CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Yannarell AC, Triplett EW (2004) Within-and between-lake variability in the composition of bacterioplankton communities: investigations using multiple spatial scales. Appl Environ Microbiol 70:214–223. CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S, Carcillo F, Chaffron S, Ignacio-Espinosa JC, Roux S, Vincent F (2015) Determinants of community structure in the global plankton interactome. Science 348:1262073–1262071–1262010. CrossRefGoogle Scholar
  42. 42.
    Chow C-ET, Kim DY, Sachdeva R, Caron DA, Fuhrman JA (2014) Top-down controls on bacterial community structure: microbial network analysis of bacteria, T4-like viruses and protists. ISME J 8:816–829. CrossRefPubMedGoogle Scholar
  43. 43.
    Kagami M, Miki T, Takimoto G (2014) Mycoloop: chytrids in aquatic food webs. Front Microbiol 5(166):161–169. CrossRefGoogle Scholar
  44. 44.
    Kasalický V, Jezbera J, Hahn MW, Šimek K (2013) The diversity of the Limnohabitans genus, an important group of freshwater bacterioplankton, by characterization of 35 isolated strains. PLoS One 8:1–13. CrossRefGoogle Scholar
  45. 45.
    Michaud L, Caruso C, Mangano S, Interdonato F, Bruni V, Lo Giudice A (2012) Predominance of Flavobacterium, Pseudomonas, and Polaromonas within the prokaryotic community of freshwater shallow lakes in the northern Victoria Land, East Antarctica. FEMS Microbiol Ecol 82:391–404. CrossRefPubMedGoogle Scholar
  46. 46.
    Middelboe M, Søndergaard M, Letarte Y, Borch N (1995) Attached and free-living bacteria: production and polymer hydrolysis during a diatom bloom. Microb Ecol 29:231–248CrossRefGoogle Scholar
  47. 47.
    Lyons M, Dobbs F (2012) Differential utilization of carbon substrates by aggregate-associated and water-associated heterotrophic bacterial communities. Hydrobiologia 686:181–193. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of MicrobiologyPusan National UniversityPusanSouth Korea
  2. 2.Division of Ecological AssessmentNational Institute of EcologySeocheonSouth Korea

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