Cutting out the middle clam: lucinid endosymbiotic bacteria are also associated with seagrass roots worldwide

Abstract

Seagrasses and lucinid bivalves inhabit highly reduced sediments with elevated sulphide concentrations. Lucinids house symbiotic bacteria (Ca. Thiodiazotropha) capable of oxidising sediment sulphide, and their presence in sediments has been proposed to promote seagrass growth by decreasing otherwise phytotoxic sulphide levels. However, vast and productive seagrass meadows are present in ecosystems where lucinids do not occur. Hence, we hypothesised that seagrasses themselves host these sulphur-oxidising Ca. Thiodiazotropha that could aid their survival when lucinids are absent. We analysed newly generated and publicly available 16S rRNA gene sequences from seagrass roots and sediments across 14 seagrass species and 10 countries and found that persistent and colonising seagrasses across the world harbour sulphur-oxidising Ca. Thiodiazotropha, regardless of the presence of lucinids. We used fluorescence in situ hybridisation to visually confirm the presence of Ca. Thiodiazotropha on roots of Halophila ovalis, a colonising seagrass species with wide geographical, water depth range, and sedimentary sulphide concentrations. We provide the first evidence that Ca. Thiodiazotropha are commonly present on seagrass roots, providing another mechanism for seagrasses to alleviate sulphide stress globally.

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Fig. 1: Global distribution of seagrass samples and the relative abundance of Ca. Thiodiazotropha.
Fig. 2: Projected images of Halophila ovalis roots (collected from the Swan River, Western Australia, Australia) with associated populations of Ca. Thiodiazotropha.

References

  1. 1.

    Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, et al. A global crisis for seagrass ecosystems. Bioscience. 2006;56:987–96.

    Article  Google Scholar 

  2. 2.

    Lamers LPM, Govers LL, Janssen ICJM, Geurts JJM, Van der Welle MEW, Van Katwijk MM, et al. Sulfide as a soil phytotoxin-a review. Front Plant Sci. 2013;4:268.

    Article  Google Scholar 

  3. 3.

    Hasler-Sheetal H, Holmer M. Sulfide intrusion and detoxification in the seagrass Zostera marina. PLoS One. 2015;10:1–19.

    Article  Google Scholar 

  4. 4.

    Brodersen KE, Lichtenberg M, Paz LC, Kühl M Epiphyte-cover on seagrass (Zostera marina L.) leaves impedes plant performance and radial O2 loss from the below-ground tissue. Front Mar Sci. 2015;2:1–11.

  5. 5.

    Fahimipour AK, Kardish MR, Lang JM, Green JL, Eisen JA, Stachowicz JJ. Global-scale structure of the eelgrass microbiome. Appl Environ Microbiol. 2017;83:1–12.

    Article  Google Scholar 

  6. 6.

    Van der Heide T, Govers LL, de Fouw J, Olff H, Van der Geest M, Van Katwijk MM, et al. A three-stage symbiosis forms the foundation of seagrass ecosystems. Science. 2012;336:1432–4.

    Article  Google Scholar 

  7. 7.

    Van Der Geest M, Van Der Heide T, Holmer M, De Wit R. First field-based evidence that the seagrass-lucinid mutualism can mitigate sulfide stress in seagrasses. Front Mar Sci. 2020;7:1–13.

    Article  Google Scholar 

  8. 8.

    Lim SJ, Alexander L, Engel AS, Paterson AT, Anderson LC, Campbell BJ. Extensive thioautotrophic gill endosymbiont diversity within a single Ctena orbiculata (Bivalvia: Lucinidae) population and implications for defining host-symbiont specificity and species recognition. mSystems. 2019;4:1–19.

    Article  Google Scholar 

  9. 9.

    Brissac T, Merçot H, Gros O. Lucinidae/sulfur-oxidizing bacteria: ancestral heritage or opportunistic association? Further insights from the Bohol Sea (the Philippines). FEMS Microbiol Ecol. 2011;75:63–76.

    CAS  Article  Google Scholar 

  10. 10.

    Brodersen KE, Koren K, Moßhammer M, Ralph PJ, Kühl M, Santner J. Seagrass-mediated phosphorus and iron solubilization in tropical sediments. Environ Sci Technol. 2017;51:14155–63.

    CAS  Article  Google Scholar 

  11. 11.

    Martin BC, Bougoure J, Ryan MH, Bennett WW, Colmer TD, Joyce NK, et al. Oxygen loss from seagrass roots coincides with colonisation of sulphide-oxidising cable bacteria and reduces sulphide stress. ISME J. 2019;13:707–19.

    CAS  Article  Google Scholar 

  12. 12.

    Callahan BJ, McMurdie PJ, Rosen M, Han AW, Johnson AJA, Holmes S. DADA2: High resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:4–5.

    Article  Google Scholar 

  13. 13.

    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–6.

    Article  Google Scholar 

  14. 14.

    Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52:696–704.

    Article  Google Scholar 

  15. 15.

    Les DH, Cleland MA, Waycott M. Phylogenetic studies in alismatidae, II: evolution of marine angiosperms (Seagrasses) and hydrophily. Am Soc Plant Taxon. 1997;22:443–63.

    Google Scholar 

  16. 16.

    Petersen JM, Kemper A, Gruber-Vodicka H, Cardini U, Van Der Geest M, Kleiner M, et al. Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation. Nat Microbiol. 2016;2:1–11.

    Google Scholar 

  17. 17.

    König S, Gros O, Heiden SE, Hinzke T, Thürmer A, Poehlein A, et al. Nitrogen fixation in a chemoautotrophic lucinid symbiosis. Nat Microbiol. 2016;2:16193.

    Article  Google Scholar 

  18. 18.

    Lim SJ, Davis BG, Gill DE, Walton J, Nachman E, Engel AS, et al. Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid species. ISME J. 2019;13:902–20.

    CAS  Article  Google Scholar 

  19. 19.

    Touchette BW, Burkholder JM. Review of nitrogen and phosphorus metabolism in seagrasses. J Exp Bot. 2000;250:133–67.

    CAS  Google Scholar 

  20. 20.

    Gros O, Liberge M, Heddi A, Khatchadourian C, Felbeck H. Detection of the free-living forms of sulfide-oxidizing gill endosymbionts in the lucinid habitat (thalassia testudinum environment). Appl Environ Microbiol. 2003;69:6264–7.

    CAS  Article  Google Scholar 

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Acknowledgements

We wish to thank Gary Kendrick, Jeremy Bougoure, Daniela Trojan, PWIS and PP for advice and fruitful discussions. MWF was supported by the Robson and Robertson postdoctoral fellowship awarded by the UWA Oceans Institute. This research was partly supported by the Integrated Coastal Analyses and Sensor Technology (ICoAST) project with funding from the Indian Ocean Marine Research Centre, a joint partnership between The University of Western Australia (UWA), the Australian Institute of Marine Science (AIMS), The Commonwealth Scientific and Industrial Research Organisation (CSIRO) and The Department of Primary Industries and Regional Development (DPIRD) WA. We also acknowledge the facilities, and the scientific and technical assistance of Microscopy Australia at the Centre for Microscopy, Characterisation & Analysis, The University of Western Australia, a facility funded by the University, State and Commonwealth Governments.

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Correspondence to Belinda C. Martin.

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Martin, B.C., Middleton, J.A., Fraser, M.W. et al. Cutting out the middle clam: lucinid endosymbiotic bacteria are also associated with seagrass roots worldwide. ISME J 14, 2901–2905 (2020). https://doi.org/10.1038/s41396-020-00771-3

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