Competition and succession among coral endosymbionts

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.

Host genotype and stable differences in algal symbiont communities explain patterns of thermal stress response ofMontipora capitatafollowing thermal pre-exposure and across multiple bleaching events

“…While previous work has established that some coral species with multi-partner symbioses can expand their thermal tolerance by "shuffling" their symbionts to change the dominant symbiont genus (Baker 2003;Silverstein et al 2014;, neither the multi-year bleaching events in 2014 and 2015 (Bahr et al 2017) nor the temperature treatments and natural thermal stress event in this study appeared to induce symbiont shuffling in M. capitata. Mixed-community colonies maintained Durusdinium-dominated symbiont communities four years post-bleaching despite the potential for a competitive advantage of Cladocopium under ambient conditions (McIlroy et al 2019). Similarly, different M. capitata genotypes with mixed communities of algal symbionts had remarkably similar Cladocopium to Durusdinium ratios.…”

“…The trends in the loss of Cladocopium from mixed-community corals may indicate some competitive advantage of Durusdinium. Previous studies have found that Durusdinium is able to outcompete Cladocopium only in thermally stressful conditions (McIlroy et al 2019), or when tradeoffs regarding growth (Jones and Berkelmans 2010;, nutrient acquisition (Baker et al 2013), and photochemical efficiency (Cantin et al 2009) diminish. Thus, the conditions of thermal stress during the mild natural warming event may have been enough to promote the preferred persistence of Durusdinium in mixed symbiont communities, but still mild enough for Cladocopium to perform relatively well in corals with no competition with Durusdinium.…”

Symbiont community diversity is more variable in corals that respond poorly to stress

“…However, this symbiont diversity may come at a cost if competitive or antagonistic interactions occur among symbiont types. Symbiont competition, which was recently documented by McIlroy et al (2019), is one potential mechanism through which destabilizing complementarity effects could have reduced symbiont benefit to worst performing hosts in this study (Miller, 2007;Moeller & Peay, 2016;Poland & Coffroth, 2019;Stanton, 2003 An alternative interpretation of the more uniform Symbiodiniaceae communities in best performing genets is that these hosts were more successful at maintaining normal physiological function under changing conditions, which could minimize stress responses by symbionts and subsequent host immune feedbacks against symbionts (e.g., Palmer, 2018). Various components of the host immune system could also contribute to the maintenance of specific symbionts in hospite (e.g., Ratzka, Gross, & Feldhaar, 2012).…”

Competitive traits of coral symbionts may alter the structure and function of the microbiome

“…Thus, rather than outcompeting C. goreaui in any scenario, it is more likely that D. trenchii is the "last man standing" as it is able to tolerate and then repopulate coral tissues under conditions unsuitable for other symbionts. In other words, this species seems well suited to proliferate only in the absence of other strains, e.g., under extreme environmental conditions [35], following bleaching [18], and in newly available host habitat [44]. Indeed, during the initial colonization of coral recruits D. trenchii often remained at lower than expected densities when other symbionts were present despite being able to fully colonize corals in their absence [44].…”