The Roles and Interactions of Symbiont, Host and Environment in Defining Coral Fitness

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2009 Jul 25

PMID 19629182

Citations 52

Authors

Jos C Mieog

Jeanine L Olsen

Ray Berkelmans

Silvia A Bleuler-Martinez

Bette L Willis

Madeleine J H van Oppen

Affiliations

Soon will be listed here.

Abstract

Background: Reef-building corals live in symbiosis with a diverse range of dinoflagellate algae (genus Symbiodinium) that differentially influence the fitness of the coral holobiont. The comparative role of symbiont type in holobiont fitness in relation to host genotype or the environment, however, is largely unknown. We addressed this knowledge gap by manipulating host-symbiont combinations and comparing growth, survival and thermal tolerance among the resultant holobionts in different environments.

Methodology/principal Findings: Offspring of the coral, Acropora millepora, from two thermally contrasting locations, were experimentally infected with one of six Symbiodinium types, which spanned three phylogenetic clades (A, C and D), and then outplanted to the two parental field locations (central and southern inshore Great Barrier Reef, Australia). Growth and survival of juvenile corals were monitored for 31-35 weeks, after which their thermo-tolerance was experimentally assessed. Our results showed that: (1) Symbiodinium type was the most important predictor of holobiont fitness, as measured by growth, survival, and thermo-tolerance; (2) growth and survival, but not heat-tolerance, were also affected by local environmental conditions; and (3) host population had little to no effect on holobiont fitness. Furthermore, coral-algal associations were established with symbiont types belonging to clades A, C and D, but three out of four symbiont types belonging to clade C failed to establish a symbiosis. Associations with clade A had the lowest fitness and were unstable in the field. Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora.

Conclusions/significance: These results highlight the complex interactions that occur between the coral host, the algal symbiont, and the environment to shape the fitness of the coral holobiont. An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change.

Citing Articles

Interspecific hybridisation provides a low-risk option for increasing genetic diversity of reef-building corals.

Lamb A, Peplow L, Dungan A, Ferguson S, Harrison P, Humphrey C Biol Open. 2024; 13(9).

PMID: 39207257 PMC: 11381923. DOI: 10.1242/bio.060482.

Chemical mutagenesis and thermal selection of coral photosymbionts induce adaptation to heat stress with trait trade-offs.

Scharfenstein H, Alvarez-Roa C, Peplow L, Buerger P, Chan W, van Oppen M Evol Appl. 2023; 16(9):1549-1567.

PMID: 37752965 PMC: 10519419. DOI: 10.1111/eva.13586.

Physiological and morphological plasticity in larvae from Eilat, Israel, to shallow and mesophotic light conditions.

Bellworthy J, Pardo R, Scucchia F, Zaslansky P, Goodbody-Gringley G, Mass T iScience. 2023; 26(7):106969.

PMID: 37534177 PMC: 10391605. DOI: 10.1016/j.isci.2023.106969.

High physiological function for corals with thermally tolerant, host-adapted symbionts.

Turnham K, Aschaffenburg M, Pettay D, Paz-Garcia D, Reyes-Bonilla H, Pinzon J Proc Biol Sci. 2023; 290(2003):20231021.

PMID: 37465983 PMC: 10354691. DOI: 10.1098/rspb.2023.1021.

Coral bleaching resistance variation is linked to differential mortality and skeletal growth during recovery.

Walker N, Nestor V, Golbuu Y, Palumbi S Evol Appl. 2023; 16(2):504-517.

PMID: 36793702 PMC: 9923480. DOI: 10.1111/eva.13500.

References

Lewis C, Coffroth M . The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science. 2004; 304(5676):1490-2. DOI: 10.1126/science.1097323. View

KINNE O . Irreversible nongenetic adaptation. Comp Biochem Physiol. 1962; 5:265-82. DOI: 10.1016/0010-406x(62)90056-7. View

Pochon X, Montoya-Burgos J, Stadelmann B, Pawlowski J . Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol. 2005; 38(1):20-30. DOI: 10.1016/j.ympev.2005.04.028. View

Iglesias-Prieto R, Beltran V, LaJeunesse T, Reyes-Bonilla H, Thome P . Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc Biol Sci. 2004; 271(1549):1757-63. PMC: 1691786. DOI: 10.1098/rspb.2004.2757. View

LaJeunesse T . "Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol. 2004; 22(3):570-81. DOI: 10.1093/molbev/msi042. View

Rowan R . Coral bleaching: thermal adaptation in reef coral symbionts. Nature. 2004; 430(7001):742. DOI: 10.1038/430742a. View

Hoegh-Guldberg O, Mumby P, Hooten A, Steneck R, Greenfield P, Gomez E . Coral reefs under rapid climate change and ocean acidification. Science. 2007; 318(5857):1737-42. DOI: 10.1126/science.1152509. View

Coffroth M, Santos S . Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist. 2005; 156(1):19-34. DOI: 10.1016/j.protis.2005.02.004. View

Abrego D, Ulstrup K, Willis B, van Oppen M . Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc Biol Sci. 2008; 275(1648):2273-82. PMC: 2603234. DOI: 10.1098/rspb.2008.0180. View

10.

Berkelmans R, van Oppen M . The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. Proc Biol Sci. 2006; 273(1599):2305-12. PMC: 1636081. DOI: 10.1098/rspb.2006.3567. View

11.

Coles S, Brown B . Coral bleaching--capacity for acclimatization and adaptation. Adv Mar Biol. 2003; 46:183-223. DOI: 10.1016/s0065-2881(03)46004-5. View

12.

Bhagooli R, Hidaka M . Photoinhibition, bleaching susceptibility and mortality in two scleractinian corals, Platygyra ryukyuensis and Stylophora pistillata, in response to thermal and light stresses. Comp Biochem Physiol A Mol Integr Physiol. 2004; 137(3):547-55. DOI: 10.1016/j.cbpb.2003.11.008. View

13.

Mieog J, van Oppen M, Berkelmans R, Stam W, Olsen J . Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Mol Ecol Resour. 2011; 9(1):74-82. DOI: 10.1111/j.1755-0998.2008.02222.x. View

14.

Day T, Nagel L, van Oppen M, Caley M . Factors affecting the evolution of bleaching resistance in corals. Am Nat. 2008; 171(2):E72-88. DOI: 10.1086/524956. View

15.

Gibert P, Huey R . Chill-coma temperature in Drosophila: effects of developmental temperature, latitude, and phylogeny. Physiol Biochem Zool. 2001; 74(3):429-34. DOI: 10.1086/320429. View

16.

Baird A, Bhagooli R, Ralph P, Takahashi S . Coral bleaching: the role of the host. Trends Ecol Evol. 2008; 24(1):16-20. DOI: 10.1016/j.tree.2008.09.005. View

17.

Tchernov D, Gorbunov M, de Vargas C, Narayan Yadav S, Milligan A, Haggblom M . Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci U S A. 2004; 101(37):13531-5. PMC: 518791. DOI: 10.1073/pnas.0402907101. View

18.

Stat M, Morris E, Gates R . Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci U S A. 2008; 105(27):9256-61. PMC: 2453720. DOI: 10.1073/pnas.0801328105. View

19.

Toller W, Rowan R, Knowlton N . Repopulation of Zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull. 2001; 201(3):360-73. DOI: 10.2307/1543614. View

20.

Jones A, Berkelmans R, van Oppen M, Mieog J, Sinclair W . A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc Biol Sci. 2008; 275(1641):1359-65. PMC: 2367621. DOI: 10.1098/rspb.2008.0069. View