Advancing coral microbiome manipulation to build long-term climate resilience
Talisa Doering A * , Justin Maire A , Madeleine J. H. van Oppen A B and Linda L. Blackall AA School of BioSciences, The University of Melbourne, Parkville, Vic., Australia.
B Australian Institute of Marine Science, Townsville, Qld, Australia.
Talisa Doering is currently a PhD student at the University of Melbourne, supervised by Prof. Madeleine J. H. van Oppen and Prof. Linda L. Blackall. She completed her Bachelor of Science degree in Biology at the Free University of Berlin, studying evolution of marine fishes to climate change regimes. She obtained her Master of Science degree in Biological Oceanography at Kiel University and GEOMAR Helmholtz Centre for Ocean Research Kiel, where she conducted a coral microbiome transplant experiment from heat-sensitive to heat-tolerant coral conspecifics in order to build coral climate resilience. Her current PhD research focuses on understanding coral bleaching mechanisms, identifying beneficial coral-associated bacteria and developing successful microbiome-manipulation approaches that can enhance coral bleaching resilience. |
Dr Justin Maire is currently a postdoctoral fellow at the University of Melbourne. He obtained his PhD in 2018 from Institut National des Sciences Appliquées de Lyon, France, on symbiotic interactions between insects and bacteria and their impact on host immunity and development. In 2019, he moved to the University of Melbourne, where his research is focused on coral–bacteria associations. He specifically focuses on closely associated symbionts, e.g. intracellular, vertically transmitted symbionts, and their potential use as bacterial probiotics and microbiome engineering as an approach for the mitigation of coral bleaching and coral reef conservation. This includes characterising the taxonomy, localisation and functions of symbionts of interests. |
Prof. Madeleine J. H. van Oppen is an ecological geneticist with an interest in microbial symbioses and climate change adaptation of reef corals. Her early career focused on evolutionary and population genetics of algae and fish, and subsequently corals. Currently, her team is using bioengineering approaches aimed at increasing coral climate resilience and the likelihood that coral reefs will survive this century. These interventions include coral host hybridisation and conditioning, directed evolution of microalgal symbionts and bacterial probiotics. |
Prof. Linda L. Blackall is an environmental microbial ecologist, who has studied many different complex microbial communities ranging from host associated through to free living in numerous environments. One of her research fields is the microbiota of corals and sponges. The numerous methods she develops and employs in her research allow elucidation of microbial complexity and function in these diverse biomes. |
Microbiology Australia 44(1) 36-40 https://doi.org/10.1071/MA23009
Submitted: 15 January 2023 Accepted: 1 March 2023 Published: 9 March 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the ASM. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Coral reefs house one-third of all marine species and are of high cultural and socioeconomic importance. However, coral reefs are under dire threat from climate change and other anthropogenic stressors. Climate change is causing coral bleaching, the breakdown of the symbiosis between the coral host and its algal symbionts, often resulting in coral mortality and the deterioration of these valuable ecosystems. While it is essential to counteract the root causes of climate change, it remains urgent to develop coral restoration and conservation methods that will buy time for coral reefs. The manipulation of the bacterial microbiome that is associated with corals has been suggested as one intervention to improve coral climate resilience. Early coral microbiome-manipulation studies, which are aimed at enhancing bleaching tolerance, have shown promising results, but the inoculated bacteria did generally not persist within the coral microbiome. Here, we highlight the importance of long-term incorporation of bacterial inocula into the microbiome of target corals, as repeated inoculations will be too costly and not feasible on large reef systems like the Great Barrier Reef. Therefore, coral microbiome-manipulation studies need to prioritise approaches that can provide sustained coral climate resilience.
Keywords: assisted evolution, coral bleaching, coral microbiome, microbiome manipulation, probiotics.
References
[1] Hoegh-Guldberg, O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50, 839–866.| Climate change, coral bleaching and the future of the world’s coral reefs.Crossref | GoogleScholarGoogle Scholar |
[2] Suggett, DJ and Smith, DJ (2020) Coral bleaching patterns are the outcome of complex biological and environmental networking. Glob Chang Biol 26, 68–79.
| Coral bleaching patterns are the outcome of complex biological and environmental networking.Crossref | GoogleScholarGoogle Scholar |
[3] Hughes, TP et al. (2021) Emergent properties in the responses of tropical corals to recurrent climate extremes. Curr Biol 31, 5393–5399.e3.
| Emergent properties in the responses of tropical corals to recurrent climate extremes.Crossref | GoogleScholarGoogle Scholar |
[4] van Oppen, MJH et al. (2015) Building coral reef resilience through assisted evolution. Proc Natl Acad Sci USA 112, 2307–2313.
| Building coral reef resilience through assisted evolution.Crossref | GoogleScholarGoogle Scholar |
[5] Damjanovic, K et al. (2017) The contribution of microbial biotechnology to mitigating coral reef degradation. Microb Biotechnol 10, 1236–1243.
| The contribution of microbial biotechnology to mitigating coral reef degradation.Crossref | GoogleScholarGoogle Scholar |
[6] Blackall, LL et al. (2015) Coral-the world’s most diverse symbiotic ecosystem. Mol Ecol 24, 5330–5347.
| Coral-the world’s most diverse symbiotic ecosystem.Crossref | GoogleScholarGoogle Scholar |
[7] Bourne, DG et al. (2016) Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu Rev Microbiol 70, 317–340.
| Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems.Crossref | GoogleScholarGoogle Scholar |
[8] Ritchie, KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322, 1–14.
| Regulation of microbial populations by coral surface mucus and mucus-associated bacteria.Crossref | GoogleScholarGoogle Scholar |
[9] Ziegler, M et al. (2017) Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Commun 8, 14213.
| Bacterial community dynamics are linked to patterns of coral heat tolerance.Crossref | GoogleScholarGoogle Scholar |
[10] Oakley CA, Davy SK (2018) Cell biology of coral bleaching. In Coral Bleaching (van Oppen M, Lough J, eds). pp. 189–211. Springer International Publishing.
[11] Wooldridge, SA (2013) Breakdown of the coral-algae symbiosis: towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae. Biogeosciences 10, 1647–1658.
| Breakdown of the coral-algae symbiosis: towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae.Crossref | GoogleScholarGoogle Scholar |
[12] Rädecker, N et al. (2021) Heat stress destabilizes symbiotic nutrient cycling in corals. Proc Natl Acad Sci USA 118, e2022653118.
| Heat stress destabilizes symbiotic nutrient cycling in corals.Crossref | GoogleScholarGoogle Scholar |
[13] Wiedenmann, J et al. (2013) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3, 160–164.
| Nutrient enrichment can increase the susceptibility of reef corals to bleaching.Crossref | GoogleScholarGoogle Scholar |
[14] Harkins, CP et al. (2020) Manipulating the human microbiome to manage disease. JAMA 323, 303–304.
| Manipulating the human microbiome to manage disease.Crossref | GoogleScholarGoogle Scholar |
[15] Damjanovic, K et al. (2019) Experimental inoculation of coral recruits with marine bacteria indicates scope for microbiome manipulation in Acropora tenuis and Platygyra daedalea. Front Microbiol 10, 1702.
| Experimental inoculation of coral recruits with marine bacteria indicates scope for microbiome manipulation in Acropora tenuis and Platygyra daedalea.Crossref | GoogleScholarGoogle Scholar |
[16] Alagely, A et al. (2011) Signaling-mediated cross-talk modulates swarming and biofilm formation in a coral pathogen Serratia marcescens. ISME J 5, 1609–1620.
| Signaling-mediated cross-talk modulates swarming and biofilm formation in a coral pathogen Serratia marcescens.Crossref | GoogleScholarGoogle Scholar |
[17] dos Santos, HF et al. (2015) Impact of oil spills on coral reefs can be reduced by bioremediation using probiotic microbiota. Sci Rep 5, 18268.
| Impact of oil spills on coral reefs can be reduced by bioremediation using probiotic microbiota.Crossref | GoogleScholarGoogle Scholar |
[18] Rosado, PM et al. (2019) Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation. ISME J 13, 921–936.
| Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation.Crossref | GoogleScholarGoogle Scholar |
[19] Santoro, EP et al. (2021) Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality. Sci Adv 7, 19–21.
| Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality.Crossref | GoogleScholarGoogle Scholar |
[20] Doering, T et al. (2021) Towards enhancing coral heat tolerance : a “microbiome transplantation” treatment using inoculations of homogenized coral tissues. Microbiome 9, 102.
| Towards enhancing coral heat tolerance : a “microbiome transplantation” treatment using inoculations of homogenized coral tissues.Crossref | GoogleScholarGoogle Scholar |
[21] Dungan, AM et al. (2022) Exploring microbiome engineering as a strategy for improved thermal tolerance in Exaiptasia diaphana. J Appl Microbiol 132, 2940–2956.
| Exploring microbiome engineering as a strategy for improved thermal tolerance in Exaiptasia diaphana.Crossref | GoogleScholarGoogle Scholar |
[22] Hernandez-Agreda, A et al. (2016) The microbial signature provides insight into the mechanistic basis of coral success across reef habitats. MBio 7, e00560-16.
| The microbial signature provides insight into the mechanistic basis of coral success across reef habitats.Crossref | GoogleScholarGoogle Scholar |
[23] Maire, J et al. (2021) Intracellular bacterial symbionts in corals: challenges and future directions. Microorganisms 9, 2209.
| Intracellular bacterial symbionts in corals: challenges and future directions.Crossref | GoogleScholarGoogle Scholar |
[24] Work, TM and Aeby, GS (2014) Microbial aggregates within tissues infect a diversity of corals throughout the Indo-Pacific. Mar Ecol Prog Ser 500, 1–9.
| Microbial aggregates within tissues infect a diversity of corals throughout the Indo-Pacific.Crossref | GoogleScholarGoogle Scholar |
[25] Flores, HA and O’Neill, SL (2018) Controlling vector-borne diseases by releasing modified mosquitoes. Nat Rev Microbiol 16, 508–518.
| Controlling vector-borne diseases by releasing modified mosquitoes.Crossref | GoogleScholarGoogle Scholar |
[26] Frommlet, JC et al. (2015) Coral symbiotic algae calcify ex hospite in partnership with bacteria. Proc Natl Acad Sci USA 112, 6158–6163.
| Coral symbiotic algae calcify ex hospite in partnership with bacteria.Crossref | GoogleScholarGoogle Scholar |
[27] Maire, J et al. (2021) Intracellular bacteria are common and taxonomically diverse in cultured and in hospite algal endosymbionts of coral reefs. ISME J 15, 2028–2042.
| Intracellular bacteria are common and taxonomically diverse in cultured and in hospite algal endosymbionts of coral reefs.Crossref | GoogleScholarGoogle Scholar |
[28] Motone, K et al. (2020) A zeaxanthin-producing bacterium isolated from the algal phycosphere protects coral endosymbionts from environmental stress. mBio 11, e01019-19.
| A zeaxanthin-producing bacterium isolated from the algal phycosphere protects coral endosymbionts from environmental stress.Crossref | GoogleScholarGoogle Scholar |
[29] Maire, J and van Oppen, MJH (2022) A role for bacterial experimental evolution in coral bleaching mitigation? Trends Microbiol 30, 217–228.
| A role for bacterial experimental evolution in coral bleaching mitigation?Crossref | GoogleScholarGoogle Scholar |
[30] Setter, RO et al. (2022) Co-occurring anthropogenic stressors reduce the timeframe of environmental viability for the world’s coral reefs. PLoS Biol 20, e3001821.
| Co-occurring anthropogenic stressors reduce the timeframe of environmental viability for the world’s coral reefs.Crossref | GoogleScholarGoogle Scholar |
