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The roles and interactions of symbiont, host and environment in defining coral fitness.

Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJ - PLoS ONE (2009)

Bottom Line: 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.Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora.An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change.

View Article: PubMed Central - PubMed

Affiliation: Australian Institute of Marine Science, Townsville, Queensland, Australia. josmieog@gmail.com

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.

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Heat-stress experiment 2: PAM-fluorometry.Effect of three different temperature regimes on the excitation pressure over photosystem II of three groups of juvenile coral outplanted to the Keppel Islands, and one outplanted to Magnetic Island. See materials and methods for nomenclature. $ = target temperature is reached, + = significant difference between KKA and MKC1/KKC1/KKD corals (p<0.001), # = significant difference between all three symbiont types (p<0.05). KKA corals responded much stronger to the heat-stress than the other three juvenile coral groups, as indicated by a sharp increase in Q values for KKA corals in the highest temperature treatment relatively early in the experiment.
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pone-0006364-g004: Heat-stress experiment 2: PAM-fluorometry.Effect of three different temperature regimes on the excitation pressure over photosystem II of three groups of juvenile coral outplanted to the Keppel Islands, and one outplanted to Magnetic Island. See materials and methods for nomenclature. $ = target temperature is reached, + = significant difference between KKA and MKC1/KKC1/KKD corals (p<0.001), # = significant difference between all three symbiont types (p<0.05). KKA corals responded much stronger to the heat-stress than the other three juvenile coral groups, as indicated by a sharp increase in Q values for KKA corals in the highest temperature treatment relatively early in the experiment.

Mentions: This experiment assessed the thermal tolerance of three coral groups outplanted to the Keppel Islands (KKA, KKC1, KKD corals) and one group outplanted to Magnetic Island (MKC1 corals). There was a strong symbiont type effect on Q under heat-stress (Fig. 4a–c and Table 1f, p<0.001). In contrast, no significant effect of outplant location was found; the KKC1 and MKC1 corals responded in a similar manner at all temperatures and time points (Table 1e). No significant differences in Q were found between the experimental groups at 27°C or 31°C (Fig. 4a, b), although at 31°C a different trend was visible for KKC1/MKC1 vs KKA and KKD. All groups responded immediately to the heating by a strong reduction in Q. Next, KKC1/MKC1 remained level for the duration of the experiment, whereas KKA and KKD showed a slow but steady increase over the next two weeks. At the highest temperature (32.5°C, Fig. 4c), all groups initially responded again with a strong reduction in Q. Next, Q rapidly increased for KKA corals after ∼1 week and approached values of 1 by the end of the experiment. This coincided with a sharp drop in maximum quantum yield (supporting information, Fig. S4), indicating severe heat-stress in the KKA group early in the experiment. Variance around the mean in Q for KKA after 9 days was relatively high, due to nine colonies within the KKA group that were less heat-stressed. These colonies were sampled at the end of the experiment, and upon genotyping, were found to harbor a residual community of type D Symbiodinium. By comparison, Q values of KKC1/MKC1 and KKD corals were much less affected by the cumulative heat-stress: KKC1/MKC1 showed a small increase at the end of the experiment, whereas KKD showed an earlier small increase and leveled out from day 11 onwards. The maximum quantum yield showed relatively small and similar reductions for KKC1/MKC1 and KKD corals (supporting information, Fig. S4).


The roles and interactions of symbiont, host and environment in defining coral fitness.

Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJ - PLoS ONE (2009)

Heat-stress experiment 2: PAM-fluorometry.Effect of three different temperature regimes on the excitation pressure over photosystem II of three groups of juvenile coral outplanted to the Keppel Islands, and one outplanted to Magnetic Island. See materials and methods for nomenclature. $ = target temperature is reached, + = significant difference between KKA and MKC1/KKC1/KKD corals (p<0.001), # = significant difference between all three symbiont types (p<0.05). KKA corals responded much stronger to the heat-stress than the other three juvenile coral groups, as indicated by a sharp increase in Q values for KKA corals in the highest temperature treatment relatively early in the experiment.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2710517&req=5

pone-0006364-g004: Heat-stress experiment 2: PAM-fluorometry.Effect of three different temperature regimes on the excitation pressure over photosystem II of three groups of juvenile coral outplanted to the Keppel Islands, and one outplanted to Magnetic Island. See materials and methods for nomenclature. $ = target temperature is reached, + = significant difference between KKA and MKC1/KKC1/KKD corals (p<0.001), # = significant difference between all three symbiont types (p<0.05). KKA corals responded much stronger to the heat-stress than the other three juvenile coral groups, as indicated by a sharp increase in Q values for KKA corals in the highest temperature treatment relatively early in the experiment.
Mentions: This experiment assessed the thermal tolerance of three coral groups outplanted to the Keppel Islands (KKA, KKC1, KKD corals) and one group outplanted to Magnetic Island (MKC1 corals). There was a strong symbiont type effect on Q under heat-stress (Fig. 4a–c and Table 1f, p<0.001). In contrast, no significant effect of outplant location was found; the KKC1 and MKC1 corals responded in a similar manner at all temperatures and time points (Table 1e). No significant differences in Q were found between the experimental groups at 27°C or 31°C (Fig. 4a, b), although at 31°C a different trend was visible for KKC1/MKC1 vs KKA and KKD. All groups responded immediately to the heating by a strong reduction in Q. Next, KKC1/MKC1 remained level for the duration of the experiment, whereas KKA and KKD showed a slow but steady increase over the next two weeks. At the highest temperature (32.5°C, Fig. 4c), all groups initially responded again with a strong reduction in Q. Next, Q rapidly increased for KKA corals after ∼1 week and approached values of 1 by the end of the experiment. This coincided with a sharp drop in maximum quantum yield (supporting information, Fig. S4), indicating severe heat-stress in the KKA group early in the experiment. Variance around the mean in Q for KKA after 9 days was relatively high, due to nine colonies within the KKA group that were less heat-stressed. These colonies were sampled at the end of the experiment, and upon genotyping, were found to harbor a residual community of type D Symbiodinium. By comparison, Q values of KKC1/MKC1 and KKD corals were much less affected by the cumulative heat-stress: KKC1/MKC1 showed a small increase at the end of the experiment, whereas KKD showed an earlier small increase and leveled out from day 11 onwards. The maximum quantum yield showed relatively small and similar reductions for KKC1/MKC1 and KKD corals (supporting information, Fig. S4).

Bottom Line: 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.Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora.An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change.

View Article: PubMed Central - PubMed

Affiliation: Australian Institute of Marine Science, Townsville, Queensland, Australia. josmieog@gmail.com

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.

Show MeSH
Related in: MedlinePlus