Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality

Erika P. Santoro; Ricardo M. Borges; Josh L. Espinoza; Marcelo Freire; Camila S. M. A. Messias; Helena D. M. Villela; Leandro M. Pereira; Caren L. S. Vilela; João G. Rosado; Pedro M. Cardoso; Phillipe M. Rosado; Juliana M. Assis; Gustavo A. S. Duarte; Gabriela Perna; Alexandre S. Rosado; Andrew Macrae; Christopher L. Dupont; Karen E. Nelson; Michael Sweet; Christian R. Voolstra; Raquel S Peixoto

doi:10.1126/sciadv.abg3088

Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality

Erika P. Santoro, Ricardo M. Borges, Josh L. Espinoza, Marcelo Freire, Camila S. M. A. Messias, Helena D. M. Villela, Leandro M. Pereira, Caren L. S. Vilela, João G. Rosado, Pedro M. Cardoso, Phillipe M. Rosado, Juliana M. Assis, Gustavo A. S. Duarte, Gabriela Perna, Alexandre S. Rosado, Andrew Macrae, Christopher L. Dupont, Karen E. Nelson, Michael Sweet, Christian R. VoolstraRaquel S Peixoto

Research output: Contribution to journal › Article › peer-review

124 Scopus citations

Abstract

Beneficial microorganisms for corals (BMCs) ameliorate environmental stress, but whether they can prevent mortality and the underlying host response mechanisms remains elusive. Here, we conducted omics analyses on the coral Mussismilia hispida exposed to bleaching conditions in a long-term mesocosm experiment and inoculated with a selected BMC consortium or a saline solution placebo. All corals were affected by heat stress, but the observed “post-heat stress disorder” was mitigated by BMCs, signified by patterns of dimethylsulfoniopropionate degradation, lipid maintenance, and coral host transcriptional reprogramming of cellular restructuration, repair, stress protection, and immune genes, concomitant with a 40% survival rate increase and stable photosynthetic performance by the endosymbiotic algae. This study provides insights into the responses that underlie probiotic host manipulation. We demonstrate that BMCs trigger a dynamic microbiome restructuring process that instigates genetic and metabolic alterations in the coral host that eventually mitigate coral bleaching and mortality.

Original language	English (US)
Pages (from-to)	eabg3088
Journal	Science advances
Volume	7
Issue number	33
DOIs	https://doi.org/10.1126/sciadv.abg3088
State	Published - Aug 13 2021

Bibliographical note

KAUST Repository Item: Exported on 2021-08-16
Acknowledged KAUST grant number(s): BAS/1/1095-01-01
Acknowledgements: This research project won the Great Barrier Reef Foundation’s Out of the Blue Box Reef Innovation Challenge People’s Choice Award supported by The Tiffany & Co.Foundation. C.R.V. was supported through the Deutsche Forschungsgemeinschaft (DFG; German Research Foundation) Project Numbers 433042944 and 458901010. R.S.P. was supported through KAUST grant number BAS/1/1095-01-01 and the Rio de Janeiro Marine Aquarium Research Center. E.P.S. received support from the Graduate Programs of Science (Microbiology) and Plant Biotechnology and Bioprocess Engineering (PBV)/Federal University of Rio de Janeiro, the Brazilian Government Research Agency CAPES, and the CAPES PRINT international mobility grant.

Access to Document

10.1126/sciadv.abg3088

https://repository.kaust.edu.sa/bitstream/10754/670602/1/eabg3088.full.pdf

Cite this

Santoro, E. P., Borges, R. M., Espinoza, J. L., Freire, M., Messias, C. S. M. A., Villela, H. D. M., Pereira, L. M., Vilela, C. L. S., Rosado, J. G., Cardoso, P. M., Rosado, P. M., Assis, J. M., Duarte, G. A. S., Perna, G., Rosado, A. S., Macrae, A., Dupont, C. L., Nelson, K. E., Sweet, M., ... Peixoto, R. S. (2021). Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality. Science advances, 7(33), eabg3088. https://doi.org/10.1126/sciadv.abg3088

@article{e4a3c9bb58ff437384585bc7e4668729,

title = "Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality",

abstract = "Beneficial microorganisms for corals (BMCs) ameliorate environmental stress, but whether they can prevent mortality and the underlying host response mechanisms remains elusive. Here, we conducted omics analyses on the coral Mussismilia hispida exposed to bleaching conditions in a long-term mesocosm experiment and inoculated with a selected BMC consortium or a saline solution placebo. All corals were affected by heat stress, but the observed “post-heat stress disorder” was mitigated by BMCs, signified by patterns of dimethylsulfoniopropionate degradation, lipid maintenance, and coral host transcriptional reprogramming of cellular restructuration, repair, stress protection, and immune genes, concomitant with a 40% survival rate increase and stable photosynthetic performance by the endosymbiotic algae. This study provides insights into the responses that underlie probiotic host manipulation. We demonstrate that BMCs trigger a dynamic microbiome restructuring process that instigates genetic and metabolic alterations in the coral host that eventually mitigate coral bleaching and mortality.",

author = "Santoro, {Erika P.} and Borges, {Ricardo M.} and Espinoza, {Josh L.} and Marcelo Freire and Messias, {Camila S. M. A.} and Villela, {Helena D. M.} and Pereira, {Leandro M.} and Vilela, {Caren L. S.} and Rosado, {Jo{\~a}o G.} and Cardoso, {Pedro M.} and Rosado, {Phillipe M.} and Assis, {Juliana M.} and Duarte, {Gustavo A. S.} and Gabriela Perna and Rosado, {Alexandre S.} and Andrew Macrae and Dupont, {Christopher L.} and Nelson, {Karen E.} and Michael Sweet and Voolstra, {Christian R.} and Peixoto, {Raquel S}",

note = "KAUST Repository Item: Exported on 2021-08-16 Acknowledged KAUST grant number(s): BAS/1/1095-01-01 Acknowledgements: This research project won the Great Barrier Reef Foundation{\textquoteright}s Out of the Blue Box Reef Innovation Challenge People{\textquoteright}s Choice Award supported by The Tiffany & Co.Foundation. C.R.V. was supported through the Deutsche Forschungsgemeinschaft (DFG; German Research Foundation) Project Numbers 433042944 and 458901010. R.S.P. was supported through KAUST grant number BAS/1/1095-01-01 and the Rio de Janeiro Marine Aquarium Research Center. E.P.S. received support from the Graduate Programs of Science (Microbiology) and Plant Biotechnology and Bioprocess Engineering (PBV)/Federal University of Rio de Janeiro, the Brazilian Government Research Agency CAPES, and the CAPES PRINT international mobility grant.",

year = "2021",

month = aug,

day = "13",

doi = "10.1126/sciadv.abg3088",

language = "English (US)",

volume = "7",

pages = "eabg3088",

journal = "Science advances",

issn = "2375-2548",

publisher = "American Association for the Advancement of Science",

number = "33",

}

Santoro, EP, Borges, RM, Espinoza, JL, Freire, M, Messias, CSMA, Villela, HDM, Pereira, LM, Vilela, CLS, Rosado, JG, Cardoso, PM, Rosado, PM, Assis, JM, Duarte, GAS, Perna, G, Rosado, AS, Macrae, A, Dupont, CL, Nelson, KE, Sweet, M, Voolstra, CR & Peixoto, RS 2021, 'Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality', Science advances, vol. 7, no. 33, pp. eabg3088. https://doi.org/10.1126/sciadv.abg3088

TY - JOUR

T1 - Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality

AU - Santoro, Erika P.

AU - Borges, Ricardo M.

AU - Espinoza, Josh L.

AU - Freire, Marcelo

AU - Messias, Camila S. M. A.

AU - Villela, Helena D. M.

AU - Pereira, Leandro M.

AU - Vilela, Caren L. S.

AU - Rosado, João G.

AU - Cardoso, Pedro M.

AU - Rosado, Phillipe M.

AU - Assis, Juliana M.

AU - Duarte, Gustavo A. S.

AU - Perna, Gabriela

AU - Rosado, Alexandre S.

AU - Macrae, Andrew

AU - Dupont, Christopher L.

AU - Nelson, Karen E.

AU - Sweet, Michael

AU - Voolstra, Christian R.

AU - Peixoto, Raquel S

N1 - KAUST Repository Item: Exported on 2021-08-16 Acknowledged KAUST grant number(s): BAS/1/1095-01-01 Acknowledgements: This research project won the Great Barrier Reef Foundation’s Out of the Blue Box Reef Innovation Challenge People’s Choice Award supported by The Tiffany & Co.Foundation. C.R.V. was supported through the Deutsche Forschungsgemeinschaft (DFG; German Research Foundation) Project Numbers 433042944 and 458901010. R.S.P. was supported through KAUST grant number BAS/1/1095-01-01 and the Rio de Janeiro Marine Aquarium Research Center. E.P.S. received support from the Graduate Programs of Science (Microbiology) and Plant Biotechnology and Bioprocess Engineering (PBV)/Federal University of Rio de Janeiro, the Brazilian Government Research Agency CAPES, and the CAPES PRINT international mobility grant.

PY - 2021/8/13

Y1 - 2021/8/13

N2 - Beneficial microorganisms for corals (BMCs) ameliorate environmental stress, but whether they can prevent mortality and the underlying host response mechanisms remains elusive. Here, we conducted omics analyses on the coral Mussismilia hispida exposed to bleaching conditions in a long-term mesocosm experiment and inoculated with a selected BMC consortium or a saline solution placebo. All corals were affected by heat stress, but the observed “post-heat stress disorder” was mitigated by BMCs, signified by patterns of dimethylsulfoniopropionate degradation, lipid maintenance, and coral host transcriptional reprogramming of cellular restructuration, repair, stress protection, and immune genes, concomitant with a 40% survival rate increase and stable photosynthetic performance by the endosymbiotic algae. This study provides insights into the responses that underlie probiotic host manipulation. We demonstrate that BMCs trigger a dynamic microbiome restructuring process that instigates genetic and metabolic alterations in the coral host that eventually mitigate coral bleaching and mortality.

AB - Beneficial microorganisms for corals (BMCs) ameliorate environmental stress, but whether they can prevent mortality and the underlying host response mechanisms remains elusive. Here, we conducted omics analyses on the coral Mussismilia hispida exposed to bleaching conditions in a long-term mesocosm experiment and inoculated with a selected BMC consortium or a saline solution placebo. All corals were affected by heat stress, but the observed “post-heat stress disorder” was mitigated by BMCs, signified by patterns of dimethylsulfoniopropionate degradation, lipid maintenance, and coral host transcriptional reprogramming of cellular restructuration, repair, stress protection, and immune genes, concomitant with a 40% survival rate increase and stable photosynthetic performance by the endosymbiotic algae. This study provides insights into the responses that underlie probiotic host manipulation. We demonstrate that BMCs trigger a dynamic microbiome restructuring process that instigates genetic and metabolic alterations in the coral host that eventually mitigate coral bleaching and mortality.

UR - http://hdl.handle.net/10754/670602

UR - https://advances.sciencemag.org/lookup/doi/10.1126/sciadv.abg3088

U2 - 10.1126/sciadv.abg3088

DO - 10.1126/sciadv.abg3088

M3 - Article

C2 - 34389536

SN - 2375-2548

VL - 7

SP - eabg3088

JO - Science advances

JF - Science advances

IS - 33

ER -

Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality

Abstract

Bibliographical note

Access to Document

Other files and links

Fingerprint

Cite this