Skip to main content
Log in

Ecological Dynamics and Co-occurrences Among Prokaryotes and Microeukaryotes in a Diatom Bloom Process in Xiangshan Bay, China

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

Abstract

Diatom blooms can significantly affect the succession of microbial communities, yet little is known about the assembly processes and interactions of microbial communities during autumn bloom events. In this study, we investigated the ecological effects of an autumn diatom bloom on prokaryotic communities (PCCs) and microeukaryotic communities (MECs), focusing on their assembly processes and interactions. The PCCs were largely dominated by Alphaproteobacteria, Gammaproteobacteria, Cyanobacteria, and Flavobacteria, while the MECs primarily included Diatomea, Dinoflagellata, and Chlorophyta. The succession of both PCCs and MECs was mainly driven by this diatom bloom and environmental factors, such as nitrate and silicate. Null modeling revealed that homogeneous selection had a more pronounced impact on the structure of PCCs compared with that of MECs. In particular, drift and dispersal limitation cannot be neglected in the assembly processes of MECs. Co-occurrence network analyses showed that Litorimicrobium, Cercozoa, Marine Group I (MGI), Cryptomonadales, Myrionecta, and Micromonas may affect the bloom process. In summary, these results elucidated the complex, robust interactions and obviously distinct assembly mechanisms of PCCs and MECs during a diatom bloom and extend our current comprehension of the ecological mechanisms and microbial interactions involved in an autumn diatom bloom process.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Data availability

All data and materials as well as software application support our published claims and comply with field standards.

Code Availability

Not applicable.

References

  1. Klindworth A, Mann AJ, Huang S, Wichels A, Quast C, Waldmann J, Teeling H, Gloeckner FO (2014) Diversity and activity of marine bacterioplankton during a diatom bloom in the North Sea assessed by total RNA and pyrotag sequencing. Mar Genom 18:185–192

    Article  Google Scholar 

  2. Suzuki K, Kuwata A, Yoshie N, Shibata A, Kawanobe K, Saito H (2011) Population dynamics of phytoplankton, heterotrophic bacteria, and viruses during the spring bloom in the western subarctic Pacific. Deep-Sea Res Pt i 58:575–589

    Article  CAS  Google Scholar 

  3. Needham DM, Fuhrman JA (2016) Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom. Nat Microbiol 1:16005

    Article  PubMed  CAS  Google Scholar 

  4. Needham DM, Sachdeva R, Fuhrman JA (2017) Ecological dynamics and co-occurrence among marine phytoplankton, bacteria and myoviruses shows microdiversity matters. ISME J 11:1614–1629

    Article  PubMed  PubMed Central  Google Scholar 

  5. Sun JY, Song Y, Ma ZP, Zhang HJ, Yang ZD, Cai ZH, Zhou J (2017) Fungal community dynamics during a marine dinoflagellate (Noctiluca scintillans) bloom. Mar Environ Res 131:183–194

    Article  PubMed  CAS  Google Scholar 

  6. Jung SW, Noh SY, Kang D, Lee TK (2017) Comparison of bacterioplankton communities between before and after inoculation with an algicidal material, Ca-aminoclay, to mitigate Cochlodinium polykrikoides blooms: assessment using microcosm experiments. J Appl Phycol 29:1343–1354

    Article  CAS  Google Scholar 

  7. Yang J, Loeder MGJ, Wiltshire KH, Montagnes DJS (2021) Comparing the Trophic impact of microzooplankton during the spring and autumn blooms in temperate waters. Estuar Coast 44:189–198

    Article  Google Scholar 

  8. RijalLeblad B, Amnhir R, Reqia S, Sitel F, Daoudi M, Marhraoui M, OueladAbdellah MK, Veron B, Er-Raioui H, Laabir M (2020) Seasonal variations of phytoplankton assemblages in relation to environmental factors in Mediterranean coastal waters of Morocco, a focus on HABs species. Harmful Algae 96:101819

    Article  CAS  Google Scholar 

  9. Zhou J, Liu W, Deng Y, Jiang YH, Xue K, He Z, Van Nostrand JD, Wu L, Yang Y, Wang A (2013) Stochastic assembly leads to alternative communities with distinct functions in a bioreactor microbial community. mBio 4:e00584-12

    Article  PubMed  PubMed Central  Google Scholar 

  10. Stegen JC, Lin X, Konopka AE, Fredrickson JK (2012) Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J 6:1653–1664

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Jiao S, Yang Y, Xu Y, Zhang J, Lu Y (2019) Balance between community assembly processes mediates species coexistence in agricultural soil microbiomes across eastern China. ISME J 14:202–216

    Article  PubMed  PubMed Central  Google Scholar 

  12. Yan Q, Stegen JC, Yu Y, Deng Y, Li X, Wu S, Dai L, Zhang X, Li J, Wang C, Ni J, Li X, Hu H, Xiao F, Feng W, Ning D, He Z, Van Nostrand JD, Wu L, Zhou J (2017) Nearly a decade-long repeatable seasonal diversity patterns of bacterioplankton communities in the eutrophic Lake Donghu (Wuhan, China). Mol Ecol 26:3839–3850

    Article  PubMed  CAS  Google Scholar 

  13. Logares R, Deutschmann IM, Junger PC, Giner CR, Krabberod AK, Schmidt TSB, Rubinat-Ripoll L, Mestre M, Salazar G, Ruiz-Gonzalez C, Sebastian M, de Vargas C, Acinas SG, Duarte CM, Gasol JM, Massana R (2020) Disentangling the mechanisms shaping the surface ocean microbiota. Microbiome 8:55

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Bio 85:183–206

    Article  Google Scholar 

  15. Chen W, Ren K, Isabwe A, Chen H, Liu M, Yang J (2019) Stochastic processes shape microeukaryotic community assembly in a subtropical river across wet and dry seasons. Microbiome 7:138

    Article  PubMed  PubMed Central  Google Scholar 

  16. Jizhong Zhou DN (2017) Stochastic community assembly: does it matter in microbial ecology? Microbiol Mol Biol R 81:e00002-00017

    Google Scholar 

  17. Dini-Andreotea F, Stegen JC, van Elsasa JD, Salles JF (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. P Natl Acad Sci USA 12:E1326–E1332

    Google Scholar 

  18. Barberan A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343–351

    Article  PubMed  CAS  Google Scholar 

  19. Eiler A, Heinrich F, Bertilsson S (2012) Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J 6:330–342

    Article  PubMed  CAS  Google Scholar 

  20. Needham DM, Chow C-ET, Cram JA, Sachdeva R, Parada A, Fuhrman JA (2013) Short-term observations of marine bacterial and viral communities: patterns, connections and resilience. ISME J 7:1274–1285

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Decaestecker E, Gaba S, Raeymaekers JAM, Stoks R, Van Kerckhoven L, Ebert D, De Meester L (2007) Host-parasite ‘Red Queen’ dynamics archived in pond sediment. Nature 450:870–873

    Article  PubMed  CAS  Google Scholar 

  22. Ma B, Wang Y, Ye S, Liu S, Stirling E, Gilbert JA, Faust K, Knight R, Jansson JK, Cardona C, Rottjers L, Xu J (2020) Earth microbial co-occurrence network reveals interconnection pattern across microbiomes. Microbiome 8:82

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Krug L, Erlacher A, Markut K, Berg G, Cernava T (2020) The microbiome of alpine snow algae shows a specific inter-kingdom connectivity and algae-bacteria interactions with supportive capacities. ISME J 14:2197–2210

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Ma B, Wang H, Dsouza M, Lou J, He Y, Dai Z, Brookes PC, Xu J, Gilbert JA (2016) Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China. ISME J 10:1891–1901

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Huo YZ, Xu SN, Wang YY, Zhang JH, Zhang YJ, Wu WN, Chen YQ, He PM (2011) Bioremediation efficiencies of Gracilaria verrucosa cultivated in an enclosed sea area of Hangzhou Bay, China. J Appl Phycol 23:173–182

    Article  Google Scholar 

  26. Hou F, Zhang H, Xie W, Zhou X, Zhu X, Zhang D (2020) Co-occurrence patterns and assembly processes of microeukaryotic communities in an early-spring diatom bloom. Sci Total Environ 711:134624

    Article  PubMed  CAS  Google Scholar 

  27. Zhang H, Wang K, Shen L, Chen H, Hou F, Zhou X, Zhang D, Zhu X (2018) Microbial community dynamics and assembly follow trajectories of an early-spring diatom bloom in a semienclosed bay. Appl Environ Microbiol 84:e01000-01018

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. AQSIQ (2007) The specification for marine monitoring of China-Part 4: seawater analysis (GB 17378.4–2007). General administration of quality supervision, inspection and quarantine (AQSIQ) of the People’s Republic of China.

  29. Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 18:1403–1414

    Article  PubMed  CAS  Google Scholar 

  30. Brate J, Logares R, Berney C, Ree DK, Klaveness D, Jakobsen KS, Shalchian-Tabrizi K (2010) Freshwater Perkinsea and marine-freshwater colonizations revealed by pyrosequencing and phylogeny of environmental rDNA. ISME J 4:1144–1153

    Article  PubMed  CAS  Google Scholar 

  31. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  PubMed  CAS  Google Scholar 

  34. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Gloeckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  PubMed  CAS  Google Scholar 

  35. Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930

    Article  Google Scholar 

  36. Kolde, (2018) pheatmap: pretty heatmaps. R Package Version 1:12

    Google Scholar 

  37. Diniz-Filho JAF, Soares TN, Lima JS, Dobrovolski R, Landeiro VL, de Campos Telles MP, Rangel TF, Bini LM (2013) Mantel test in population genetics. Genet Mol Biol 36:475–485

    Article  PubMed  PubMed Central  Google Scholar 

  38. Dufrene M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366

    Google Scholar 

  39. Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, Rockhold ML, Konopka A (2013) Quantifying community assembly processes and identifying features that impose them. ISME J 7:2069–2079

    Article  PubMed  PubMed Central  Google Scholar 

  40. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  PubMed  CAS  Google Scholar 

  41. Csárdi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 1695:1–9

    Google Scholar 

  42. Shannon P, Markiel A, Ozier O, Baliga N, Wang J, 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Bastian M HS, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. Int Conf Weblogs Soc Media.

  44. Zhang H, Hou F, Xie W, Wang K, Zhou X, Zhang D, Zhu X (2020) Interaction and assembly processes of abundant and rare microbial communities during a diatom bloom process. Environ Microbiol 22:1707–1719

    Article  PubMed  CAS  Google Scholar 

  45. Boyd PW, Strzepek R, Chiswell S, Chang H, Hutchins DA (2012) Microbial control of diatom bloom dynamics in the open ocean. Geophys Res Lett 39:L18601

    Article  Google Scholar 

  46. Taylor JD, Cottingham SD, Billinge J, Cunliffe M (2014) Seasonal microbial community dynamics correlate with phytoplankton-derived polysaccharides in surface coastal waters. ISME J 8:245–248

    Article  PubMed  CAS  Google Scholar 

  47. Cunliffe M, Engel A, Frka S, Gasparovic B, Guitart C, Murrell JC, Salter M, Stolle C, Upstill-Goddard R, Wurl O (2013) Sea surface microlayers: a unified physicochemical and biological perspective of the air-ocean interface. Prog Oceanogr 109:104–116

    Article  Google Scholar 

  48. 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

    Article  PubMed  CAS  Google Scholar 

  49. Giner CR, Balague V, Krabberod AK, Ferrera I, Rene A, Garces E, Gasol JM, Logares R, Massana R (2019) Quantifying long-term recurrence in planktonic microbial eukaryotes. Mol Ecol 28:923–935

    Article  PubMed  Google Scholar 

  50. Li H, Xing P, Chen M, Bian Y, Wu QL (2011) Short-term bacterial community composition dynamics in response to accumulation and breakdown of Microcystis blooms. Water Res 45:1702–1710

    Article  PubMed  CAS  Google Scholar 

  51. Stevens H, Ulloa O (2008) Bacterial diversity in the oxygen minimum zone of the eastern tropical South Pacific. Environ Microbiol 10:1244–1259

    Article  PubMed  CAS  Google Scholar 

  52. Monier A, Comte J, Babin M, Forest A, Matsuoka A, Lovejoy C (2015) Oceanographic structure drives the assembly processes of microbial eukaryotic communities. ISME J 9:990–1002

    Article  PubMed  CAS  Google Scholar 

  53. Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704–726

    Article  Google Scholar 

  54. Giovannoni SJ (2017) SAR11 Bacteria: the most abundant plankton in the oceans. Annu Rev Mar 9:231–255

    Article  Google Scholar 

  55. Stingl U, Desiderio RA, Cho JC, Vergin KL, Giovannoni SJ (2007) The SAR92 clade: an abundant coastal clade of culturable marine bacteria possessing proteorhodopsin. Appl Environ Microb 73:2290–2296

    Article  CAS  Google Scholar 

  56. Hoarfrost A, Nayfach S, Ladau J, Yooseph S, Arnosti C, Dupont CL, Pollard KS (2020) Global ecotypes in the ubiquitous marine clade SAR86. ISME J 14:178–188

    Article  PubMed  CAS  Google Scholar 

  57. Richardson J, Miller C, Maberly SC, Taylor P, Globevnik L, Hunter P, Jeppesen E, Mischke U, Moe SJ, Pasztaleniec A, Sondergaard M, Carvalho L (2018) Effects of multiple stressors on cyanobacteria abundance vary with lake type. Global Change Biol 24:5044–5055

    Article  Google Scholar 

  58. Alonso C, Warnecke F, Amann R, Pernthaler J (2007) High local and global diversity of Flavobacteria in marine plankton. Environ Microbiol 9:1253–1266

    Article  PubMed  CAS  Google Scholar 

  59. Tinta T, Vojvoda J, Mozetic P, Talaber I, Vodopivec M, Malfatti F, Turk V (2015) Bacterial community shift is induced by dynamic environmental parameters in a changing coastal ecosystem (northern Adriatic, northeastern Mediterranean Sea) - a 2-year time-series study. Environ Microbiol 17:3581–3596

    Article  PubMed  CAS  Google Scholar 

  60. Zhou ZX, Yu RC, Zhou MJ (2017) Resolving the complex relationship between harmful algal blooms and environmental factors in the coastal waters adjacent to the Changjiang River estuary. Harmful Algae 62:60–72

    Article  PubMed  Google Scholar 

  61. Piwosz K, Spich K, Calkiewicz J, Weydmann A, Kubiszyn AM, Wiktor JM (2015) Distribution of small phytoflagellates along an Arctic fjord transect. Environ Microbiol 17:2393–2406

    Article  PubMed  Google Scholar 

  62. Fuhrman JA, Cram JA, Needham DM (2015) Marine microbial community dynamics and their ecological interpretation. Nat Rev Microbiol 13:133–146

    Article  PubMed  CAS  Google Scholar 

  63. Wang Y, Pan J, Yang J, Zhou Z, Pan Y, Li M (2020) Patterns and processes of free-living and particle-associated bacterioplankton and archaeaplankton communities in a subtropical river-bay system in South China. Limnol Oceanogr 65:S161–S179

    Article  Google Scholar 

  64. Jiang ZB, Chen QZ, Zeng JN, Liao YB, Shou L, Liu J (2012) Phytoplankton community distribution in relation to environmental parameters in three aquaculture systems in a Chinese subtropical eutrophic bay. Mar Ecol Prog Ser 446:73–89

    Article  CAS  Google Scholar 

  65. Bie TD, Meester LD, Brendonck L, Martens K, Goddeeris B, Ercken D, Hampel H, Denys L, Vanhecke L, Gucht KVD (2012) Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecol Lett 15:740–747

    Article  PubMed  Google Scholar 

  66. Matcher G, Lemley DA, Adams JB (2021) Bacterial community dynamics during a harmful algal bloom of Heterosigma akashiwo. Aquat Microb Ecol 86:153–167

    Article  Google Scholar 

  67. Berdjeb L, Parada A, Needham DM, Fuhrman JA (2018) Short-term dynamics and interactions of marine protist communities during the spring-summer transition. ISME J 12:1907–1917

    Article  PubMed  PubMed Central  Google Scholar 

  68. Peacock EE, Olson RJ, Sosik HM (2014) Parasitic infection of the diatom Guinardia delicatula, a recurrent and ecologically important phenomenon on the New England Shelf. Mar Ecol Prog Ser 503:1–10

    Article  Google Scholar 

  69. Lambert S, Lozano J-C, Bouget F-Y, Galand PE (2021) Seasonal marine microorganisms change neighbors under contrasting environmental conditions. Environ Microbiol 23:2592–2604

    Article  PubMed  Google Scholar 

  70. Johnson M, Stoecker DK (2005) Role of feeding in growth and photophysiology of Myrionecta rubra. Aquat Microb Ecol 39:303–312

    Article  Google Scholar 

  71. Sañudo-Wilhelmy S, Gómez-Consarnau L, Suffridge C, Webb E (2014) The role of B vitamins in marine biogeochemistry. Annu Rev Mar Sci 6:339–367

    Article  Google Scholar 

  72. Kim S, Kang YG, Kim HS, Yih W, Coats DW, Park MG (2008) Growth and grazing responses of the mixotrophic dinoflagellate Dinophysis acuminata as functions of light intensity and prey concentration. Aquat Microb Ecol 51:301–310

    Article  Google Scholar 

  73. Brannock PM, Ortmann AC, Moss AG, Halanych KM (2016) Metabarcoding reveals environmental factors influencing spatio-temporal variation in pelagic micro-eukaryotes. Mol Ecol 25:3593–3604

    Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (42076158, 41706132), the Fundamental Research Funds for the Provincial Universities of Zhejiang (SJLY2020005), and K.C. Wong Magna Fund in Ningbo University.

Author information

Authors and Affiliations

Authors

Contributions

Methodology, data analysis, writing—original draft: Weijuan Xie; investigation, methodology, data analysis, preparation: Yi Yan; visualization, investigation: Jian Hu; methodology, data analysis: Pengsheng Dong; software, validation: Dandi Hou; funding acquisition, writing—reviewing and editing, supervision: Huajun Zhang; validation, visualization: Zhiyuan Yao; investigation, preparation: Xiangyu Zhu; writing—reviewing and editing, supervision: Demin Zhang.

Corresponding authors

Correspondence to Huajun Zhang or Demin Zhang.

Ethics declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Conflict of Interest

The authors declare no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 11918 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xie, W., Yan, Y., Hu, J. et al. Ecological Dynamics and Co-occurrences Among Prokaryotes and Microeukaryotes in a Diatom Bloom Process in Xiangshan Bay, China. Microb Ecol 84, 746–758 (2022). https://doi.org/10.1007/s00248-021-01899-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-021-01899-1

Keywords

Navigation