Academic Journal
Ocean warming indirectly affects seagrass performance through effects on sediment microbial communities.
| Τίτλος: | Ocean warming indirectly affects seagrass performance through effects on sediment microbial communities. |
|---|---|
| Συγγραφείς: | Jongen R; School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, 2006, Australia., Gribben PE; School of Biological Earth and Environmental Sciences, Centre for Marine Science and Innovation, University of New South Wales, Sydney, NSW, 2052, Australia., Erickson KR; School of Biological Earth and Environmental Sciences, Centre for Marine Science and Innovation, University of New South Wales, Sydney, NSW, 2052, Australia., Marzinelli EM; School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, 2006, Australia. |
| Πηγή: | The New phytologist [New Phytol] 2026 Jul; Vol. 251 (1), pp. 191-206. Date of Electronic Publication: 2026 May 05. |
| Τύπος έκδοσης: | Journal Article |
| Γλώσσα: | English |
| Στοιχεία περιοδικού: | Publisher: Wiley on behalf of New Phytologist Trust Country of Publication: England NLM ID: 9882884 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1469-8137 (Electronic) Linking ISSN: 0028646X NLM ISO Abbreviation: New Phytol Subsets: MEDLINE |
| Imprint Name(s): | Publication: Oxford : Wiley on behalf of New Phytologist Trust Original Publication: London, New York [etc.] Academic Press. |
| Ιατρικοί όροι (MeSH): | Geologic Sediments*/microbiology , Zosteraceae*/microbiology , Zosteraceae*/physiology , Zosteraceae*/growth & development , Oceans and Seas* , Global Warming* , Microbiota*, Rhizosphere ; Biomass ; Temperature ; Bacteria |
| Περίληψη: | Belowground microbes are increasingly recognised as mediators of plant responses to stress, but it remains unclear whether the thermal histories of marine plants and their associated belowground microbes influence plant performance under ocean warming. We conducted a common-garden field experiment at a long-term warmed site in Lake Macquarie (NSW, Australia, > 30 yr, 1-3°C warming), to test the effects of sediment origin (ambient vs warm-origin), plant origin (ambient vs warm-origin) and microbial disruption (intact vs disrupted rhizosphere and bulk sediment microbial communities) on seagrass (Zostera muelleri) performance. Both plant origins had lower aboveground biomass in intact warm-origin sediments, but warm-origin plants recovered when bulk sediment microbial communities were disrupted, indicating that warming-altered sediment microbial communities can suppress seagrass performance. Disrupted warm-origin sediments were enriched in sulphide-oxidising bacteria, which likely contributed to enhanced performance. In warm-origin sediments, rhizosphere bacterial communities were similar across plant origins, indicating that sediments shape rhizosphere bacterial assembly. Rhizosphere microbial disruption had no effect on plant performance. We show that ocean warming can shape sediment microbial communities in ways that suppress seagrass performance, suggesting that sediment microbial communities can override plant thermal history and act as hidden constraints on seagrass tolerance to warming. (© 2026 The Author(s). New Phytologist © 2026 New Phytologist Foundation.) |
| References: | Anderson MJ. 2001. A new method for non‐parametric multivariate analysis of variance. Austral Ecology 26: 32–46. Anderson MJ, Ellingsen KE, McArdle BH. 2006. Multivariate dispersion as a measure of beta diversity. Ecology Letters 9: 683–693. Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed‐effects models using lme4. Journal of Statistical Software 67: 1. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B, Methodological 57: 289–300. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. 2016. Dada2: high‐resolution sample inference from Illumina amplicon data. Nature Methods 13: 7. Calvin K, Dasgupta D, Krinner G, Mukherji A, Thorne PW, Trisos C, Romero J, Aldunce P, Barrett K, Blanco G. 2023. IPCC, 2023: climate change 2023: synthesis report. In: Core Writing Team, Lee H, Romero J, eds. Contribution of working groups I, II and III to the sixth assessment report of the Intergovernmental Panel on Climate Change. Geneva, Switzerland: IPCC. Chefaoui RM, Duarte CM, Serrão EA. 2018. Dramatic loss of seagrass habitat under projected climate change in the Mediterranean Sea. Global Change Biology 24: 4919–4928. Coleman MA, Wood G, Filbee‐Dexter K, Minne AJP, Goold HD, Vergés A, Marzinelli EM, Steinberg PD, Wernberg T. 2020. Restore or redefine: future trajectories for restoration. Frontiers in Marine Science 7: 237. CSIRO, & BOM. 2015. Climate change in Australia: information for Australia's natural resource management regions. Technical report. Cullen‐Unsworth L, Unsworth R. 2013. Seagrass meadows, ecosystem services, and sustainability. Environment: Science and Policy for Sustainable Development 55: 14–28. Davis NM, Proctor DM, Holmes SP, Relman DA, Callahan BJ. 2018. Simple statistical identification and removal of contaminant sequences in marker‐gene and metagenomics data. Microbiome 6: 226. DCCEEW. 2024. Synthesis report. Assessment of surface water and sediment quality in the vicinity of power stations and coal ash repositories in Lake Macquarie, NSW. Department of Climate Change, Energy, the Environment and Water, Paramatta, NSW, Australia. De Boeck HJ, Hiltbrunner E, Verlinden M, Bassin S, Zeiter M. 2018. Legacy effects of climate extremes in alpine grassland. Frontiers in Plant Science 9: 1586. Dyksma S, Pester M. 2024. Growth of sulfate‐reducing desulfobacterota and Bacillota at periodic oxygen stress of 50% air‐O2 saturation. Microbiome 12: 191. Eyre B. 2005. Lake Macquarie water quality review: 2001–2005. Southern Cross University, Centre for Coastal Biogeochemistry, Lismore, Australia. Ferretto G, Glasby TM, Poore AGB, Callaghan CT, Housefield GP, Langley M, Sinclair EA, Statton J, Kendrick GA, Vergés A. 2021. Naturally‐detached fragments of the endangered seagrass Posidonia australis collected by citizen scientists can be used to successfully restore fragmented meadows. Biological Conservation 262: 109308. Fox J, Weisberg S, Adler D, Bates D, Baud‐Bovy G, Ellison S, Firth D, Friendly M, Gorjanc G, Graves S. 2012. Package ‘car’. Vienna, Austria: R Foundation for Statistical Computing, 16. Fuggle RE, Gribben PE, Marzinelli EM. 2023. Experimental evidence root‐associated microbes mediate seagrass response to environmental stress. Journal of Ecology 111: 1079–1093. Garthwin RG, Poore AGB, Vergés A. 2014. Seagrass tolerance to herbivory under increased ocean temperatures. Marine Pollution Bulletin, Seagrass Meadows in a Globally Changing Environment 83: 475–482. Gribben PE, Nielsen S, Seymour JR, Bradley DJ, West MN, Thomas T. 2017. Microbial communities in marine sediments modify success of an invasive macrophyte. Scientific Reports 7: 9845. Gull A, Lone AA, Wani NUI, Gull A, Lone AA, Wani NUI. 2019. Biotic and abiotic stresses in plants. In: Bosco de Oliveira A, ed. Abiotic and biotic stress in plants. London, UK: IntechOpen. doi: 10.5772/intechopen.85832. Hasler‐Sheetal H, Holmer M. 2015. Sulfide intrusion and detoxification in the seagrass Zostera marina. PLoS ONE 10: e0129136. Ingleton T, McMinn A. 2012. Thermal plume effects: a multi‐disciplinary approach for assessing effects of thermal pollution on estuaries using benthic diatoms and satellite imagery. Estuarine, Coastal and Shelf Science 99: 132–144. Jensen SI, Kühl M, Priemé A. 2007. Different bacterial communities associated with the roots and bulk sediment of the seagrass Zostera marina. FEMS Microbiology Ecology 62: 108–117. Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM. 2010. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proceedings of the National Academy of Sciences, USA 107: 2093–2098. Jongen R, Marzinelli EM, Bugnot AB, Ferguson A, Fraser MW, Glasby TM, Jackson EL, Martin BC, Sherman CDH, Sinclair EA et al. 2024. Integrating belowground interactions into seagrass restoration strategies. In: Oceanography and marine biology. CRC Press: Taylor & Francis, 192–214. Jongen R, Marzinelli EM, Vadillo Gonzalez S, Hart JL, Kjelleberg S, Gribben PE. 2025. Contrasting effects of rhizosphere and sediment microbiota on seagrass performance in response to a simulated marine heatwave. Journal of Ecology 113: 2429–2446. Kardish MR, Stachowicz JJ. 2023. Local environment drives rapid shifts in composition and phylogenetic clustering of seagrass microbiomes. Scientific Reports 13: 3673. Kerr EA, Strother S. 1989. Seasonal changes in leaf growth rate of Zostera muelleri Irmisch ex Aschers. In South‐Eastern Australia. Aquatic Botany 33: 131–140. Khan MA, Asaf S, Khan AL, Jan R, Kang S‐M, Kim K‐M, Lee I‐J. 2020. Extending thermotolerance to tomato seedlings by inoculation with SA1 isolate of Bacillus cereus and comparison with exogenous humic acid application. PLoS ONE 15: e0232228. Lau JA, Lennon JT. 2012. Rapid responses of soil microorganisms improve plant fitness in novel environments. Proceedings of the National Academy of Sciences, USA 109: 14058–14062. Lin H, Peddada SD. 2020. Analysis of compositions of microbiomes with bias correction. Nature Communications 11: 3514. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA‐seq data with DESeq2. Genome Biology 15: 550. McGrath AH, Lema K, Egan S, Wood G, Gonzalez SV, Kjelleberg S, Steinberg PD, Marzinelli EM. 2024. Disentangling direct vs indirect effects of microbiome manipulations in a habitat‐forming marine holobiont. npj Biofilms and Microbiomes 10: 1–12. McMurdie PJ, Holmes S. 2013. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8: e61217. Moir T, Huggett MJ, Kirkman T, Smith TM, Gaston TF. 2025. Decadal long sub‐lethal temperature increases alter the production of non‐structural carbohydrates in Zostera muelleri. Marine Environmental Research 208: 107124. Nielsen JT, Liesack W, Finster K. 1999. Desulfovibrio zosterae sp. Nov., a new sulfate reducer isolated from surface‐sterilized roots of the seagrass Zostera marina. International Journal of Systematic and Evolutionary Microbiology 49: 859–865. Nimbs MJ, Glasby TM, Sinclair EA, Swadling D, Davis TR, Coleman MA. 2024. A donor registry: genomic analyses of Posidonia australis seagrass meadows identifies adaptive genotypes for future‐proofing. Ecology and Evolution 14: e70667. Parks DH, Chuvochina M, Chaumeil P‐A, Rinke C, Mussig AJ, Hugenholtz P. 2020. A complete domain‐to‐species taxonomy for bacteria and archaea. Nature Biotechnology 38: 9. Petipas RH, Geber MA, Lau JA. 2021. Microbe‐mediated adaptation in plants. Ecology Letters 24: 1302–1317. Petipas RH, Wruck AC, Geber MA. 2020. Microbe‐mediated local adaptation to limestone barrens is context dependent. Ecology 101: e03092. Piercey RS, Gribben PE, Hanley TC, Moles AT, Hughes AR. 2021. Incorporating marine macrophytes in plant–soil feedbacks: emerging evidence and opportunities to advance the field. Journal of Ecology 109: 614–625. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2012. The SILVA ribosomal RNA gene database project: improved data processing and web‐based tools. Nucleic Acids Research 41(D1): D590–D596. Revillini D, David AS, Menges ES, Main KN, Afkhami ME, Searcy CA. 2022. Microbiome‐mediated response to pulse fire disturbance outweighs the effects of fire legacy on plant performance. New Phytologist 233: 2071–2082. Rojas‐Tapias D, Moreno‐Galván A, Pardo‐Díaz S, Obando M, Rivera D, Bonilla R. 2012. Effect of inoculation with plant growth‐promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays). Applied Soil Ecology, Microorganisms and the Sustainable Management of Soil 61: 264–272. Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R et al. 2015. Improved plant resistance to drought is promoted by the root‐associated microbiome as a water stress‐dependent trait. Environmental Microbiology 17: 316–331. Seymour JR, Laverock B, Nielsen DA, Trevathan‐Tackett SM, Macreadie PI. 2018. The microbiology of seagrasses. In: Larkum AWD, Kendrick GA, Ralph PJ, eds. Seagrasses of Australia: structure, ecology and conservation. Cham, Switzerland: Springer International, 343–392. doi: 10.1007/978‐3‐319‐71354‐0_12. Sherman CD, York PH, Smith TM, Macreadie PI. 2016. Fine‐scale patterns of genetic variation in a widespread clonal seagrass species. Marine Biology 163: 82. Silverstein MR, Segrè D, Bhatnagar JM. 2023. Environmental microbiome engineering for the mitigation of climate change. Global Change Biology 29: 2050–2066. Smale DA, Wernberg T, Peck LS, Barnes DKA. 2011. Turning on the heat: ecological response to simulated warming in the sea. PLoS ONE 6: e16050. Swadling DS, Taylor SL, Gruber RK, Glasby TM. 2025. Sediment properties and seagrass density influence the morphological plasticity of seagrass Zostera muelleri more than elevated temperatures. Estuaries and Coasts 48: 52. Vadillo Gonzalez S, Hurd CL, Britton D, Bennett E, Steinberg PD, Marzinelli EM. 2024. Effects of temperature and microbial disruption on juvenile kelp Ecklonia radiata and its associated bacterial community. Frontiers in Marine Science 10: 1332501. doi: 10.3389/fmars.2023.1332501. Vadillo Gonzalez S, Jongen R, Thomas T, Marzinelli EM, Gribben PE. 2025. Seagrass–microbe interactions: a systematic review of current research trends and mapping of the core microbiome. Biological Reviews. doi: 10.1002/brv.70126. Van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA et al. 2013. Plant–soil feedbacks: the past, the present and future challenges. Journal of Ecology 101: 265–276. de Vries F, Lau J, Hawkes C, Semchenko M. 2023. Plant–soil feedback under drought: does history shape the future? Trends in Ecology & Evolution 38: 708–718. de Vries FT, Liiri ME, Bjørnlund L, Setälä HM, Christensen S, Bardgett RD. 2012. Legacy effects of drought on plant growth and the soil food web. Oecologia 170: 821–833. Walker LDA, Gribben P, Glasby T, Marzinelli EM, Varkey D, Dafforn K. 2024. Above and below‐ground bacterial communities shift in seagrass beds with warming temperatures. Frontiers in Marine Science 11: 1374946. Wang L, Tomas F, Mueller RS. 2020. Nutrient enrichment increases size of Zostera marina shoots and enriches for sulfur and nitrogen cycling bacteria in root‐associated microbiomes. FEMS Microbiology Ecology 96: fiaa129. Wei B, Zhang D, Wang G, Liu Y, Li Q, Zheng Z, Yang G, Peng Y, Niu K, Yang Y. 2023. Experimental warming altered plant functional traits and their coordination in a permafrost ecosystem. New Phytologist 240: 1802–1816. Welsh DT. 2000. Nitrogen fixation in seagrass meadows: regulation, plant–bacteria interactions and significance to primary productivity. Ecology Letters 3: 58–71. |
| Grant Information: | DP240100566 Australian Research Council; LP200200220 Australian Research Council |
| Contributed Indexing: | Keywords: Zostera muelleri; belowground processes; environmental change; holobiont; host–microbe interactions; microbiome; plant–soil feedbacks |
| Entry Date(s): | Date Created: 20260505 Date Completed: 20260604 Latest Revision: 20260604 |
| Update Code: | 20260605 |
| DOI: | 10.1111/nph.71195 |
| PMID: | 42084538 |
| Βάση Δεδομένων: | MEDLINE |
καταχωρήστε σχόλιο πρώτοι!