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Not just who, but how many: the importance of partner abundance in reef coral symbioses.

Cunning R, Baker AC - Front Microbiol (2014)

Bottom Line: The performance and function of reef corals depends on the genetic identity of their symbiotic algal partners, with some symbionts providing greater benefits (e.g., photosynthate, thermotolerance) than others.We suggest that symbiont abundance is a fundamental aspect of the dynamic interface between reef corals and the abiotic environment that ultimately determines the benefits, costs, and functional responses of these symbioses.In this article, we generate testable hypotheses regarding the importance of symbiont abundance by first discussing different metrics and their potential links to symbiosis performance and breakdown, and then describing how natural variability and dynamics of symbiont communities may help explain ecological patterns on coral reefs and predict responses to environmental change.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric Science, University of Miami Miami, FL, USA.

ABSTRACT
The performance and function of reef corals depends on the genetic identity of their symbiotic algal partners, with some symbionts providing greater benefits (e.g., photosynthate, thermotolerance) than others. However, these interaction outcomes may also depend on partner abundance, with differences in the total number of symbionts changing the net benefit to the coral host, depending on the particular environmental conditions. We suggest that symbiont abundance is a fundamental aspect of the dynamic interface between reef corals and the abiotic environment that ultimately determines the benefits, costs, and functional responses of these symbioses. This density-dependent framework suggests that corals may regulate the size of their symbiont pool to match microhabitat-specific optima, which may contribute to the high spatiotemporal variability in symbiont abundance observed within and among colonies and reefs. Differences in symbiont standing stock may subsequently explain variation in energetics, growth, reproduction, and stress susceptibility, and may mediate the impacts of environmental change on these outcomes. However, the importance of symbiont abundance has received relatively little recognition, possibly because commonly-used metrics based on surface area (e.g., symbiont cells cm(-2)) may be only weakly linked to biological phenomena and are difficult to compare across studies. We suggest that normalizing symbionts to biological host parameters, such as units of protein or numbers of host cells, will more clearly elucidate the functional role of symbiont abundance in reef coral symbioses. In this article, we generate testable hypotheses regarding the importance of symbiont abundance by first discussing different metrics and their potential links to symbiosis performance and breakdown, and then describing how natural variability and dynamics of symbiont communities may help explain ecological patterns on coral reefs and predict responses to environmental change.

No MeSH data available.


Related in: MedlinePlus

Theoretical costs and benefits to the coral host as a function of symbiont abundance. Net benefit equals the gross benefit minus gross cost, and the point at which net benefit is maximized is defined as the optimal symbiont abundance for the coral (Cunning, 2013; sensuHolland et al., 2002). Different sets of abiotic (light and temperature) or biotic factors (coral and symbiont type) will alter these functions (e.g., A vs. B) such that a particular optimal abundance exists for a particular set of conditions. Note that in (A), the optimal symbiont abundance is lower than in (B), but the corresponding net benefit is higher. Within either set of conditions, symbiont abundances above or below the optimum result in decreasing net benefit. Net benefits may be predictive of energetic status, growth rates, or reproductive output.
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Figure 2: Theoretical costs and benefits to the coral host as a function of symbiont abundance. Net benefit equals the gross benefit minus gross cost, and the point at which net benefit is maximized is defined as the optimal symbiont abundance for the coral (Cunning, 2013; sensuHolland et al., 2002). Different sets of abiotic (light and temperature) or biotic factors (coral and symbiont type) will alter these functions (e.g., A vs. B) such that a particular optimal abundance exists for a particular set of conditions. Note that in (A), the optimal symbiont abundance is lower than in (B), but the corresponding net benefit is higher. Within either set of conditions, symbiont abundances above or below the optimum result in decreasing net benefit. Net benefits may be predictive of energetic status, growth rates, or reproductive output.

Mentions: While incident light may be directly influenced by symbiont abundance, light absorption and quenching involve additional layers of photobiology, and downstream impacts on symbiosis function are further mediated by host-symbiont cellular interactions. Nevertheless, these complex outcomes may still be linked to symbiont abundance and illustrated within a conceptual framework (Figure 2). For example, if each symbiont provides some photosynthate, increasing symbiont abundance will increase the total photosynthate received (i.e., the gross benefit to the coral). However, at high abundances, self-shading and/or carbon-limitation may reduce photosynthesis in each cell, causing gross benefit to decline (Figure 2). This relationship is supported empirically by P:R ratios in corals that initially increase as a function of symbiont abundance (per mg protein) and subsequently decline (Hoogenboom et al., 2010). Importantly, the impact of photosynthate delivery on the coral depends on the amount of coral tissue receiving it, suggesting that symbiont abundance may better predict gross benefit when normalized to host biological parameters (e.g., protein, cell).


Not just who, but how many: the importance of partner abundance in reef coral symbioses.

Cunning R, Baker AC - Front Microbiol (2014)

Theoretical costs and benefits to the coral host as a function of symbiont abundance. Net benefit equals the gross benefit minus gross cost, and the point at which net benefit is maximized is defined as the optimal symbiont abundance for the coral (Cunning, 2013; sensuHolland et al., 2002). Different sets of abiotic (light and temperature) or biotic factors (coral and symbiont type) will alter these functions (e.g., A vs. B) such that a particular optimal abundance exists for a particular set of conditions. Note that in (A), the optimal symbiont abundance is lower than in (B), but the corresponding net benefit is higher. Within either set of conditions, symbiont abundances above or below the optimum result in decreasing net benefit. Net benefits may be predictive of energetic status, growth rates, or reproductive output.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4120693&req=5

Figure 2: Theoretical costs and benefits to the coral host as a function of symbiont abundance. Net benefit equals the gross benefit minus gross cost, and the point at which net benefit is maximized is defined as the optimal symbiont abundance for the coral (Cunning, 2013; sensuHolland et al., 2002). Different sets of abiotic (light and temperature) or biotic factors (coral and symbiont type) will alter these functions (e.g., A vs. B) such that a particular optimal abundance exists for a particular set of conditions. Note that in (A), the optimal symbiont abundance is lower than in (B), but the corresponding net benefit is higher. Within either set of conditions, symbiont abundances above or below the optimum result in decreasing net benefit. Net benefits may be predictive of energetic status, growth rates, or reproductive output.
Mentions: While incident light may be directly influenced by symbiont abundance, light absorption and quenching involve additional layers of photobiology, and downstream impacts on symbiosis function are further mediated by host-symbiont cellular interactions. Nevertheless, these complex outcomes may still be linked to symbiont abundance and illustrated within a conceptual framework (Figure 2). For example, if each symbiont provides some photosynthate, increasing symbiont abundance will increase the total photosynthate received (i.e., the gross benefit to the coral). However, at high abundances, self-shading and/or carbon-limitation may reduce photosynthesis in each cell, causing gross benefit to decline (Figure 2). This relationship is supported empirically by P:R ratios in corals that initially increase as a function of symbiont abundance (per mg protein) and subsequently decline (Hoogenboom et al., 2010). Importantly, the impact of photosynthate delivery on the coral depends on the amount of coral tissue receiving it, suggesting that symbiont abundance may better predict gross benefit when normalized to host biological parameters (e.g., protein, cell).

Bottom Line: The performance and function of reef corals depends on the genetic identity of their symbiotic algal partners, with some symbionts providing greater benefits (e.g., photosynthate, thermotolerance) than others.We suggest that symbiont abundance is a fundamental aspect of the dynamic interface between reef corals and the abiotic environment that ultimately determines the benefits, costs, and functional responses of these symbioses.In this article, we generate testable hypotheses regarding the importance of symbiont abundance by first discussing different metrics and their potential links to symbiosis performance and breakdown, and then describing how natural variability and dynamics of symbiont communities may help explain ecological patterns on coral reefs and predict responses to environmental change.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric Science, University of Miami Miami, FL, USA.

ABSTRACT
The performance and function of reef corals depends on the genetic identity of their symbiotic algal partners, with some symbionts providing greater benefits (e.g., photosynthate, thermotolerance) than others. However, these interaction outcomes may also depend on partner abundance, with differences in the total number of symbionts changing the net benefit to the coral host, depending on the particular environmental conditions. We suggest that symbiont abundance is a fundamental aspect of the dynamic interface between reef corals and the abiotic environment that ultimately determines the benefits, costs, and functional responses of these symbioses. This density-dependent framework suggests that corals may regulate the size of their symbiont pool to match microhabitat-specific optima, which may contribute to the high spatiotemporal variability in symbiont abundance observed within and among colonies and reefs. Differences in symbiont standing stock may subsequently explain variation in energetics, growth, reproduction, and stress susceptibility, and may mediate the impacts of environmental change on these outcomes. However, the importance of symbiont abundance has received relatively little recognition, possibly because commonly-used metrics based on surface area (e.g., symbiont cells cm(-2)) may be only weakly linked to biological phenomena and are difficult to compare across studies. We suggest that normalizing symbionts to biological host parameters, such as units of protein or numbers of host cells, will more clearly elucidate the functional role of symbiont abundance in reef coral symbioses. In this article, we generate testable hypotheses regarding the importance of symbiont abundance by first discussing different metrics and their potential links to symbiosis performance and breakdown, and then describing how natural variability and dynamics of symbiont communities may help explain ecological patterns on coral reefs and predict responses to environmental change.

No MeSH data available.


Related in: MedlinePlus