Skip to main content

Advertisement

SpringerLink
Log in

Consistency and Variation in the Kelp Microbiota: Patterns of Bacterial Community Structure Across Spatial Scales

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

Abstract

Kelp species are distributed along ~ 25% of the world’s coastlines and the forests they form represent some of the world’s most productive and diverse ecosystems. Like other marine habitat–formers, the associated microbial community is fundamental for host and, in turn, wider ecosystem functioning. Given there are thousands of bacteria-host associations, determining which relationships are important remains a major challenge. We characterised the associated bacteria of two habitat-forming kelp species, Laminaria hyperborea and Saccharina latissima, from eight sites across a range of spatial scales (10 s of metres to 100 s of km) in the northeast Atlantic. We found no difference in diversity or community structure between the two kelps, but there was evidence of regional structuring (across 100 s km) and considerable variation between individuals (10 s of metres). Within sites, individuals shared few amplicon sequence variants (ASVs) and supported a very small proportion of diversity found across the wider study area. However, consistent characteristics between individuals were observed with individual host communities containing a small conserved “core” (8–11 ASVs comprising 25 and 32% of sample abundances for L. hyperborea and S. latissima, respectively). At a coarser taxonomic resolution, communities were dominated by four classes (Planctomycetes, Gammaproteobacteria, Alphaproteobacteria and Bacteroidia) that made up ~ 84% of sample abundances. Remaining taxa (47 classes) made up very little contribution to overall abundance but the majority of taxonomic diversity. Overall, our study demonstrates the consistent features of kelp bacterial communities across large spatial scales and environmental gradients and provides an ecologically meaningful baseline to track environmental change.

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

Similar content being viewed by others

Data Accessibility

Sequences are accessible through the EMBL database (accession no. PRJEB50679). ASV table and metadata are available at (https://doi.org/10.6084/m9.figshare.19453889.v1).

References

  1. Nyholm SV, Graf J (2012) Knowing your friends: Invertebrate innate immunity fosters beneficial bacterial symbioses. Nat Rev Microbiol 10:815–827

    Article  CAS  PubMed  Google Scholar 

  2. Adair KL, Douglas AE (2017) Making a microbiome: the many determinants of host-associated microbial community composition. Curr Opin Microbiol 35:23–29

    Article  PubMed  Google Scholar 

  3. Beinart RA (2019) The Significance of Microbial Symbionts in Ecosystem Processes. mSystems 4:e00129-19

    Article  Google Scholar 

  4. Rosenberg E, Koren O, Reshef L et al (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    Article  CAS  PubMed  Google Scholar 

  5. Egan S, Gardiner M (2016) Microbial dysbiosis: Rethinking disease in marine ecosystems. Front Microbiol 7:991

    Article  PubMed  PubMed Central  Google Scholar 

  6. Zozaya-Valdés E, Roth-Schulze AJ, Egan S, Thomas T (2017) Microbial community function in the bleaching disease of the marine macroalgae Delisea pulchra. Environ Microbiol 19:3012–3024

    Article  PubMed  Google Scholar 

  7. Hurtado-McCormick V, Kahlke T, Petrou K et al (2021) Corrigendum: Regional and Microenvironmental Scale Characterization of the Zostera muelleri Seagrass Microbiome. Front Microbiol 12:40

    Article  Google Scholar 

  8. Simon JC, Marchesi JR, Mougel C, Selosse MA (2019) Host-microbiota interactions: From holobiont theory to analysis. Microbiome 7:1–5

    Article  Google Scholar 

  9. Sweet MJ, Bulling MT (2017) On the importance of the microbiome and pathobiome in coral health and disease. Front Mar Sci 4:9

    Article  Google Scholar 

  10. Costanza R, de Groot R, Sutton P et al (2014) Changes in the global value of ecosystem services. Glob Environ Chang 26:152–158

    Article  Google Scholar 

  11. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Ecosystem management. New York Press, p 130–147

  12. Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235–246

    Article  Google Scholar 

  13. Wilkins LGE, Leray M, O’Dea A et al (2019) Host-associated microbiomes drive structure and function of marine ecosystems. PLoS Biol 17:e3000533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ellison AM, Bank MS, Clinton BD et al (2005) Loss of foundation species: Consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486

    Article  Google Scholar 

  15. Byers JE, Cuddington K, Jones CG et al (2006) Using ecosystem engineers to restore ecological systems. Trends Ecol Evol 21:493–500

    Article  PubMed  Google Scholar 

  16. Crain CM, Bertness MD (2006) Ecosystem engineering across environmental gradients: Implications for conservation and management. Bioscience 56:211–218

    Article  Google Scholar 

  17. Angelini C, Altieri AH, Silliman BR, Bertness MD (2011) Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. Bioscience 61:782–789

    Article  Google Scholar 

  18. Mills JG, Weinstein P, Gellie NJC et al (2017) Urban habitat restoration provides a human health benefit through microbiome rewilding: the Microbiome Rewilding Hypothesis. Restor Ecol 25:866–872

    Article  Google Scholar 

  19. Wernberg T, Krumhansl K, Filbee-Dexter K, Pedersen MF (2018) Status and trends for the world’s kelp forests. In: World Seas: An Environmental Evaluation Volume III: Ecological Issues and Environmental Impacts

  20. Jayathilake DRM, Costello MJ (2020) A modelled global distribution of the kelp biome. Biol Cons 252:108815

    Article  Google Scholar 

  21. Dayton PK (1985) Ecology of kelp communities. Annu Rev Ecol Syst 16:215–230

    Article  Google Scholar 

  22. Steneck RS, Graham MH, Bourque BJ et al (2002) Kelp forest ecosystems: Biodiversity, stability, resilience and future. Environ Conserv 29:436–459

    Article  Google Scholar 

  23. Egan S, Harder T, Burke C et al (2013) The seaweed holobiont: Understanding seaweed-bacteria interactions. FEMS Microbiol Rev 37:462–476

    Article  CAS  PubMed  Google Scholar 

  24. Michel G, Nyval-Collen P, Barbeyron T et al (2006) Bioconversion of red seaweed galactans: A focus on bacterial agarases and carrageenases. Appl Microbiol Biotechnol 71:23–33

    Article  CAS  PubMed  Google Scholar 

  25. Hehemann JH, Boraston AB, Czjzek M (2014) A sweet new wave: Structures and mechanisms of enzymes that digest polysaccharides from marine algae. Curr Opin Struct Biol 28:77–86

    Article  CAS  PubMed  Google Scholar 

  26. Pfister CA, Altabet MA, Weigel BL (2019) Kelp beds and their local effects on seawater chemistry, productivity, and microbial communities. Ecology 100:e02798

    Article  PubMed  Google Scholar 

  27. Lemay MA, Davis KM, Martone PT, Parfrey LW (2021) Kelp-associated Microbiota are Structured by Host Anatomy. J Phycol 57:1119–1130

    Article  CAS  PubMed  Google Scholar 

  28. Bengtsson MM, Sjøtun K, Lanzén A, Øvreås L (2012) Bacterial diversity in relation to secondary production and succession on surfaces of the kelp Laminaria hyperborea. ISME J 6:2188–2198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Weigel BL, Pfister CA (2019) Successional dynamics and seascape-level patterns of microbial communities on the canopy-forming kelps Nereocystis luetkeana and Macrocystis pyrifera. Front Microbiol 10:346

    Article  PubMed  PubMed Central  Google Scholar 

  30. Marzinelli EM, Campbell AH, Zozaya Valdes E et al (2015) Continental-scale variation in seaweed host-associated bacterial communities is a function of host condition, not geography. Environ Microbiol 17:4078–4088

    Article  PubMed  Google Scholar 

  31. Phelps CM, McMahon K, Bissett A et al (2021) The surface bacterial community of an Australian kelp shows cross-continental variation and relative stability within regions. FEMS Microbiol Ecol 97:fiab089

    Article  CAS  PubMed  Google Scholar 

  32. Kain JM (1979) A view of the genus Laminaria. Oceanogr Mar Biol Annu Rev 17:101–161

    Google Scholar 

  33. Jupp BP, Drew EA (1974) Studies on the growth of Laminaria hyperborea (Gunn.) Fosl. I. Biomass and productivity. J Exp Mar Biol Ecol 15:185–196

    Article  Google Scholar 

  34. Kain JM (2022) The biology of Laminaria hyperborea X. The effect of depth on some populations. J Mar Biol Assoc U K 57:587–607

    Article  Google Scholar 

  35. Staufenberger T, Thiel V, Wiese J, Imhoff JF (2008) Phylogenetic analysis of bacteria associated with Laminaria saccharina. FEMS Microbiol Ecol 64:65–77

    Article  CAS  PubMed  Google Scholar 

  36. Bengtsson MM, Øvreås L (2010) Planctomycetes dominate biofilms on surfaces of the kelp Laminaria hyperborea. BMC Microbiol 10:1–12

    Article  Google Scholar 

  37. Tourneroche A, Lami R, Burgaud G et al (2020) The Bacterial and Fungal Microbiota of Saccharina latissima (Laminariales, Phaeophyceae). Front Mar Sci 0:1081

  38. Pessarrodona A, Moore PJ, Sayer MDJ, Smale DA (2018) Carbon assimilation and transfer through kelp forests in the NE Atlantic is diminished under a warmer ocean climate. Glob Chang Biol 24:4386–4398

    Article  PubMed  PubMed Central  Google Scholar 

  39. Smale DA, Burrows MT, Evans AJ et al (2016) Linking environmental variables with regional scale variability in ecological structure and standing stock of carbon within UK kelp forests. Mar Ecol Prog Ser 542:79–95

    Article  CAS  Google Scholar 

  40. Teagle H, Hawkins SJ, Moore PJ, Smale DA (2017) The role of kelp species as biogenic habitat formers in coastal marine ecosystems. J Exp Mar Biol Ecol 492:81–98

    Article  Google Scholar 

  41. Michelou VK, Caporaso JG, Knight R, Palumbi SR (2013) The Ecology of Microbial Communities Associated with Macrocystis pyrifera. PLoS ONE 8:e67480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Lemay MA, Martone PT, Keeling PJ et al (2018) Sympatric kelp species share a large portion of their surface bacterial communities. Environ Microbiol 20:658–670

    Article  PubMed  Google Scholar 

  43. Kozich JJ, Westcott SL, Baxter NT et al (2013) Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform. Appl Environ Microbiol 79:5112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Callahan BJ, Sankaran K, Fukuyama JA et al (2016) Bioconductor Workflow for Microbiome Data Analysis: from raw reads to community analyses. F1000Research 5:1492

  45. Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590

    Article  CAS  PubMed  Google Scholar 

  46. McMurdie PJ, Holmes S (2013) Phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS ONE 8:e61217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265–270

    Google Scholar 

  48. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  49. Oksanen J, Blanchet FG, Friendly M et al (2019) Package “vegan” Title Community Ecology Package. Community ecology package 2

  50. Qiu Z, Coleman MA, Provost E et al (2019) Future climate change is predicted to affect the microbiome and condition of habitat-forming kelp. Proc R Soc B 286:201887

    Article  Google Scholar 

  51. Ramirez-Puebla ST, Weigel BL, Jack L et al (2020) Spatial organization of the kelp microbiome at micron scales. bioRxiv 2020.03.01.972083

  52. Bonthond G, Bayer T, Krueger-Hadfield SA et al (2020) How do microbiota associated with an invasive seaweed vary across scales? Mol Ecol 29:2094–2108

    Article  PubMed  Google Scholar 

  53. Brown MV, Lauro FM, Demaere MZ et al (2012) Global biogeography of SAR11 marine bacteria. Mol Syst Biol 8:595

    Article  PubMed  PubMed Central  Google Scholar 

  54. Gilbert JA, Steele JA, Caporaso JG et al (2012) Defining seasonal marine microbial community dynamics. ISME J 6:298–308

    Article  CAS  PubMed  Google Scholar 

  55. Ghiglione JF, Galand PE, Pommier T et al (2012) Pole-to-pole biogeography of surface and deep marine bacterial communities. Proc Natl Acad Sci USA 109:17633–17638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Burke C, Thomas T, Lewis M et al (2011) Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 5:590–600

    Article  CAS  PubMed  Google Scholar 

  57. Sale PF (1978) (1978) Coexistence of coral reef fishes — a lottery for living space. Environ Biol Fish 3:85–102

    Article  Google Scholar 

  58. Sjøtun K (1993) Seasonal Lamina Growth in two Age Groups of Laminaria saccharina (L.) Lamour. in Western Norway. Bot Mar 36:433–442

    Article  Google Scholar 

  59. Roitman S, López-Londoño T, Joseph Pollock F et al (2020) Surviving marginalized reefs: assessing the implications of the microbiome on coral physiology and survivorship. Coral Reefs 39:795–807

    Article  Google Scholar 

  60. Wood G, Steinberg PD, Campbell AH et al (2022) Host genetics, phenotype and geography structure the microbiome of a foundational seaweed. Mol Ecol 31:2189–2206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Meusnier I, Olsen JL, Stam WT et al (2001) Phylogenetic analyses of Caulerpa taxifolia (Chlorophyta) and of its associated bacterial microflora provide clues to the origin of the Mediterranean introduction. Mol Ecol 10:931–946

    Article  CAS  PubMed  Google Scholar 

  62. Longford SR, Tujula NA, Crocetti GR et al (2007) Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquat Microb Ecol 48:217–229

    Article  Google Scholar 

  63. Lachnit T, Blümel M, Imhoff JF, Wahl M (2009) Specific epibacterial communities on macroalgae: Phylogeny matters more than habitat. Aquat Biol 5:181–186

    Article  Google Scholar 

  64. Bondoso J, Godoy-Vitorino F, Balagué V et al (2017) Epiphytic Planctomycetes communities associated with three main groups of macroalgae. FEMS Microbiol Ecol 93:fiw255

    Article  PubMed  PubMed Central  Google Scholar 

  65. Wegner CE, Richter-Heitmann T, Klindworth A et al (2013) Expression of sulfatases in Rhodopirellula baltica and the diversity of sulfatases in the genus Rhodopirellula. Mar Genomics 9:51–61

    Article  PubMed  Google Scholar 

  66. Hernandez-Agreda A, Leggat W, Bongaerts P et al (2018) Rethinking the coral microbiome: Simplicity exists within a diverse microbial biosphere. MBio 9:e00812-e818

    Article  PubMed  PubMed Central  Google Scholar 

  67. Capistrant-Fossa KA, Morrison HG, Engelen AH et al (2021) The microbiome of the habitat-forming brown alga Fucus vesiculosus (Phaeophyceae) has similar cross-Atlantic structure that reflects past and present drivers1. J Phycol 57:1681–1698

    Article  CAS  PubMed  Google Scholar 

  68. Park S, Jung YT, Won SM et al (2014) Granulosicoccus undariae sp. nov., a member of the family Granulosicoccaceae isolated from a brown algae reservoir and emended description of the genus Granulosicoccus. Antonie van Leeuwenhoek Int J Gen Mol Microbiol 106:845–852

    Article  Google Scholar 

  69. Ihua MW, FitzGerald JA, Guiheneuf F et al (2020) Diversity of bacteria populations associated with different thallus regions of the brown alga Laminaria digitata. PLoS ONE 15:e0242675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Zhang R, Chang L, Xiao L et al (2020) Diversity of the epiphytic bacterial communities associated with commercially cultivated healthy and diseased Saccharina japonica during the harvest season. J Appl Phycol 32:2071–2080

    Article  CAS  Google Scholar 

  71. Abraham WR, Rohde M (2014) The family Hyphomonadaceae. In: The Prokaryotes: Alphaproteobacteria and Betaproteobacteria, p 283–229

  72. Baek K, Choi A, Kang I et al (2014) Granulosicoccus marinus sp. nov., isolated from Antarctic seawater, and emended description of the genus Granulosicoccus. Int J Syst Evol Microbiol 64:4103–4108

    Article  PubMed  Google Scholar 

  73. Lamy T, Reed DC, Rassweiler A et al (2018) Scale-specific drivers of kelp forest communities. Oecologia 186:217–233

    Article  PubMed  Google Scholar 

  74. Rosman JH, Monismith SG, Denny MW, Koseff JR (2010) Currents and turbulence within a kelp forest (Macrocystis pyrifera): Insights from a dynamically scaled laboratory model. Limnol Oceanogr 55:1145–1158

    Article  Google Scholar 

  75. Michel J, Kaiser MJ, Attrill MJ et al (2011) Marine ecology: processes, systems, and impacts. Oxford University Press

    Google Scholar 

  76. Florez JZ, Camus C, Hengst MB, Buschmann AH (2017) A functional perspective analysis of macroalgae and epiphytic bacterial community interaction. Front Microbiol 8:2561

    Article  PubMed  PubMed Central  Google Scholar 

  77. Schiener P, Black KD, Stanley MS, Green DH (2015) The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol 27:363–373

    Article  CAS  Google Scholar 

  78. Silberfeld T, Leigh JW, Verbruggen H et al (2010) A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): Investigating the evolutionary nature of the “brown algal crown radiation.” Mol Phylogenet Evol 56:659–674

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Tritonia Scientific Ltd for providing logistical support and past and current members of the UK Team Kelp for insightful discussions and productive field trips.

Funding

D.A.S. was supported by a UKRI Future Leaders Fellowship (MR/S032827/1). P.J.M. was supported by NERC grant NE/S011692/1.

Author information

Authors and Affiliations

  1. Marine Biological Association of the United Kingdom, The Laboratory, Plymouth, PL1 2PB, UK

    Nathan G. King & Dan A. Smale

  2. School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, NE1 7RU, UK

    Pippa J. Moore

  3. Centre of Applied Marine Sciences, School of Ocean Sciences, Bangor University, Menai Bridge, LL59 5AB, UK

    Jamie M. Thorpe

Authors
  1. Nathan G. King
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pippa J. Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jamie M. Thorpe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dan A. Smale
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

PJM and DAS designed the experiment. NGK and JT conducted all laboratory work and analysis. NGK lead the manuscript preparation and all authors contributed equally to subsequent edits. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Nathan G. King.

Ethics declarations

Ethics Approval

No approval of research ethics committees was required to accomplish the goals of this study because experimental work was conducted on unregulated kelp species.

Conflict of Interest

The authors declare no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2780 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

King, N.G., Moore, P.J., Thorpe, J.M. et al. Consistency and Variation in the Kelp Microbiota: Patterns of Bacterial Community Structure Across Spatial Scales. Microb Ecol 85, 1265–1275 (2023). https://doi.org/10.1007/s00248-022-02038-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-022-02038-0

Keywords

Search

Navigation