This site needs JavaScript to work properly. Please enable it to take advantage of the complete set of features!
Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

NIH NLM Logo
Log in
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2019 Oct 30;9(22):12767-12778.
doi: 10.1002/ece3.5749. eCollection 2019 Nov.

Competition and succession among coral endosymbionts

Affiliations

Competition and succession among coral endosymbionts

Shelby E McIlroy et al. Ecol Evol. .

Abstract

Host species often support a genetically diverse guild of symbionts, the identity and performance of which can determine holobiont fitness under particular environmental conditions. These symbiont communities are structured by a complex set of potential interactions, both positive and negative, between the host and symbionts and among symbionts. In reef-building corals, stable associations with specific symbiont species are common, and we hypothesize that this is partly due to ecological mechanisms, such as succession and competition, which drive patterns of symbiont winnowing in the initial colonization of new generations of coral recruits. We tested this hypothesis using the experimental framework of the de Wit replacement series and found that competitive interactions occurred among symbionts which were characterized by unique ecological strategies. Aposymbiotic octocoral recruits within high- and low-light environments were inoculated with one of three Symbiodiniaceae species as monocultures or with cross-paired mixtures, and we tracked symbiont uptake using quantitative genetic assays. Priority effects, in which early colonizers excluded competitive dominants, were evidenced under low light, but these early opportunistic species were later succeeded by competitive dominants. Under high light, a more consistent competitive hierarchy was established in which competitive dominants outgrew and limited the abundance of others. These findings provide insight into mechanisms of microbial community organization and symbiosis breakdown and recovery. Furthermore, transitions in competitive outcomes across spatial and temporal environmental variation may improve lifetime host fitness.

Keywords: Symbiodineaceae; competition; microbiome; succession; symbiosis.

PubMed Disclaimer

Conflict of interest statement

All authors declare that there are no competing financial interests in relation to the work described.

Figures

Figure 1
Figure 1
de Wit replacement series model for symbiont competition. Two potential symbiont species are offered at ratios of 1:0, 0.5:0.5, or 0:1. In‐hospite densities of each symbiont species measured within monocultures (circles) are used to model expected in‐hospite densities in the absence of competition (dashed lines). Within duoculture, measured in‐hospite densities that fall near (gray square) or significantly below (black square) expected values signify the absence or presence of competition, respectively
Figure 2
Figure 2
Experimental set up. (a) Aposymbiotic, single polyp recruits of Briareum asbestinum were settled onto dead gorgonian branches. (b) Those branches were distributed among the high‐light and low‐light treatments within a symbiont treatment tank. Cultured Symbiodinium (A only, B only, D only, A and B, A and D, B and D) was added to tanks at 200 cells/ml. Water was continuously circulated through both light and dark chambers by a small pump and water tubing into both light chambers. (c) Treatment tanks were replicated and distributed within a water table with chilled water circulating on the outside of tanks to maintain ambient seawater temperatures. Natural lighting was modulated by a shade cloth
Figure 3
Figure 3
Mean number of symbionts per individual host (Briareum asbestinum) recruits in the (a) absence and (b) presence of competition. Low‐light (gray) and high‐light (gold) treatments at 6 weeks (left panel) and at 8 weeks (right panel) following initial inoculation of newly settled recruits. Symbiodinium microadriaticum (S. mic.), Breviolum minutum (B. min), Durusdinium trenchii (D. tren.). Data were log transformed, the geometric mean calculated and back transformed. Error bars represent back transformed 95% confidence intervals. An ANOVA indicated a significant effect of light (small letters) and symbiont (large letters) treatments on symbiont densities within the 6‐week treatment. No significant difference was observed within the 8‐week treatment
Figure 4
Figure 4
In‐hospite symbiont densities (cells per recruit) within single and mixed inoculation treatments. Each symbiont treatment was carried out under both high‐ and low‐light conditions (columns) with data collected at 6 weeks (left panel) and 8 weeks (right panel) following initial inoculation; note different scales on y‐axis. X‐axis labels show the relative ratio of each symbiont type available for uptake; Symbiodinium microadriaticum (S. mic.), Breviolum minutum (B. min), Durusdinium trenchii (D. tren.). Dashed lines show expectations of the de Wit model based on densities within the single inoculations (see Figure 1). Significant deviations are noted with asterisks, and the letters and arrows in the upper left of the graph indicate direction of deviation within the given symbiont type. Error bars show standard error of the mean
Figure 5
Figure 5
Summary of competitive hierarchy for Symbiodiniaceae species competing for symbiosis with Briareum asbestinum. Arrows go from competitive dominants to inferiors based on paired, mixed inoculation treatments under two light environments. Dashed gray connections indicate no significant influence of the presence of one species on the other. Competitive exclusion occurred where one symbiont type completely excluded another (summarized from Table 1), whereas competitive dominance was determined when one species was numerically dominant over the other (detailed from Figure 4). Competitive outcomes were tested at both 6 weeks and 8 weeks following initial inoculations. Symbiodinium microadriaticum (S. mic.), Breviolum minutum (B. min), Durusdinium trenchii (D. tren.)

References

    1. Abrego, D. , Van Oppen, M. J. H. , & Willis, B. L. (2009). Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny. Molecular Ecology, 18, 3532–3543. - PubMed
    1. Afkhami, M. E. , Rudgers, J. A. , & Stachowicz, J. J. (2014). Multiple mutualist effects: Conflict and synergy in multispecies mutualisms. Ecology, 95, 833–844. 10.1890/13-1010.1 - DOI - PubMed
    1. Baker, A. C. (2001). Ecosystems: Reef corals bleach to survive change. Nature, 411, 765–766. 10.1038/35081151 - DOI - PubMed
    1. Baker, A. (2003). Flexibility and specificity in coral‐algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium . Annual Review of Ecology Evolution and Systematics, 34, 661–689.
    1. Baker, A. , Starger, C. , McClanahan, T. , & Glynn, P. (2004). Corals' adaptive response to climate change. Nature, 430, 741–741. 10.1038/430741a - DOI - PubMed

LinkOut - more resources

Cite

AltStyle によって変換されたページ (->オリジナル) /