For ecosystems vulnerable to environmental change, understanding the spatiotemporal stability of functionally crucial symbioses is fundamental to determining the mechanisms by which these ecosystems may persist. The coral Pachyseris speciosa is a successful environmental generalist that succeeds in diverse reef habitats. The generalist nature of this coral suggests it may have the capacity to form functionally significant microbial partnerships to facilitate access to a range of nutritional sources within different habitats. Here, we propose that coral is a metaorganism hosting three functionally distinct microbial interactions: a ubiquitous core microbiome of very few symbiotic host-selected bacteria, a microbiome of spatially and/or regionally explicit core microbes filling functional niches (<100 phylotypes), and a highly variable bacterial community that is responsive to biotic and abiotic processes across spatial and temporal scales (>100,000 phylotypes). We find that this coral hosts upwards of 170,000 distinct phylotypes and provide evidence for the persistence of a select group of bacteria in corals across environmental habitats of the Great Barrier Reef and Coral Sea. We further show that a higher number of bacteria are consistently associated with corals on mesophotic reefs than on shallow reefs. An increase in microbial diversity with depth suggests reliance by this coral on bacteria for nutrient acquisition on reefs exposed to nutrient upwelling. Understanding the complex microbial communities of host organisms across broad biotic and abiotic environments as functionally distinct microbiomes can provide insight into those interactions that are ubiquitous niche symbioses and those that provide competitive advantage within the hosts’ environment.
We propose that the coral holobiont should be conceptualized as a diverse transient microbial community that is responsive to the surrounding environment and encompasses a simple, redundant, resident microbiome and a small conserved core microbiome. Most importantly, we show that the coral microbiome is comparable to the microbiomes of other organisms studied thus far. Accurately characterizing the coral-microbe interactions provides an important baseline from which the functional roles and the functional niches within which microbes reside can be deciphered.
Research into the microbiomes of natural environments is changing the way ecologists and evolutionary biologists view the importance of microbes in ecosystem function. This is particularly relevant in ocean environments, where microbes constitute the majority of biomass and control most of the major biogeochemical cycles, including those that regulate the Earth's climate. Coastal marine environments provide goods and services that are imperative to human survival and well-being (e.g. fisheries, water purification), and emerging evidence indicates that these ecosystem services often depend on complex relationships between communities of microorganisms (the 'microbiome') and their hosts or environment -termed the 'holobiont'. Understanding of coastal ecosystem function must therefore be framed under the holobiont concept, whereby macroorganisms and their associated microbiomes are considered as a synergistic ecological unit. Here we evaluated the current state of knowledge on coastal marine microbiome research and identified key questions within this growing research area. Although the list of questions is broad and ambitious, progress in the field is increasing exponentially, and the emergence of large, international collaborative networks and well-executed manipulative experiments are rapidly advancing the field of coastal marine microbiome research.
Coral microbiomes are critical to holobiont health and functioning, but the stability of host–microbial interactions is fragile, easily shifting from eubiosis to dysbiosis. The heat-induced breakdown of the symbiosis between the host and its dinoflagellate algae (that is, “bleaching”), is one of the most devastating outcomes for reef ecosystems. Yet, bleaching tolerance has been observed in some coral species. This review provides an overview of the holobiont’s diversity, explores coral thermal tolerance in relation to their associated microorganisms, discusses the hypothesis of adaptive dysbiosis as a mechanism of environmental adaptation, mentions potential solutions to mitigate bleaching, and suggests new research avenues. More specifically, we define coral bleaching as the succession of three holobiont stages, where the microbiota can (i) maintain essential functions for holobiont homeostasis during stress and/or (ii) act as a buffer to mitigate bleaching by favoring the recruitment of thermally tolerant Symbiodiniaceae species (adaptive dysbiosis), and where (iii) environmental stressors exceed the buffering capacity of both microbial and dinoflagellate partners leading to coral death.
In the last two decades, over 100 studies have investigated the structure of the coral microbiome. However, as yet there are no standardized methods applied to sample preservation and preparation, with different studies using distinct methods. There have also been several comparisons made of microbiome data generated across different studies, which have not addressed the influence of the methodology employed over each of the microbiome datasets. Here, we assess three different preservation methods; salt saturated dimethyl sulfoxide (DMSO) – EDTA, snap freezing with liquid nitrogen and 4% paraformaldehyde solution, and two different preparation methodologies; bead beating and crushing, that have been applied to study the coral microbiome. We compare the resultant bacterial assemblage data for two coral growth forms, the massive coral Goniastrea edwardsi and the branching coral Isopora palifera. We show that microbiome datasets generated from differing preservation and processing protocols are comparable in composition (presence/absence). Significant discrepancies between preservation and homogenization methods are observed in structure (relative abundance), and in the occurrence and dominance of taxa, with rare (low abundance and low occurrence) phylotypes being the most variable fraction of the microbial community. Finally, we provide evidence to support chemical preservation with DMSO as effective as snap freezing samples for generating reliable and robust microbiome datasets. In conclusion, we recommend where possible a standardized preservation and extraction method be taken up by the field to provide the best possible practices for detailed assessments of symbiotic and conserved bacterial associations.
Aim We evaluated whether patterns of species diversity (α, β and γ) of rocky shore assemblages followed latitudinal gradients (i.e. LDGs) along the South American coasts, and tested hypotheses related to potential processes sustaining or disrupting the expected LDG pattern at various spatial scales. Location Coasts of South America. Taxon Macroalgae and sessile/slow‐moving macrofauna on intertidal rocky shores. Methods We evaluated changes in species composition across 143 sites. The degree of replacement and loss of species at different spatial scales (i.e. coasts, regions and sites) were estimated to help distinguish among ecological, historical and evolutionary hypotheses for explaining LDGs. Furthermore, components of diversity and taxonomic distinctness were measured, and variability in these measures was decomposed using analysis of covariance. Finally, we examined relationships between diversity and a suite of environmental and anthropogenic variables to identify potential mechanisms that may be responsible for the reported spatial relationships. Results Species composition varied with latitude, and this variability was relatively consistent on both coasts. At all spatial scales, replacement of species was the dominant phenomenon (>95%), rather than loss in the total number of species (<5%). LDGs were strongly dependent on the diversity component and the spatial scale: generally, positive for regional β‐diversity, negative for α‐diversity and site β‐diversity. Sea surface temperature (SST) was the variable that best explained patterns of diversity along both coasts (14%–22%), but other regional and local environmental variables associated with river discharges, upwelling, confluence of currents, tides and anthropogenic pressures also accounted for an important portion of variation (5%–14% each). Main conclusions Species diversity of South American rocky shores followed, with interruptions, LDGs. The trend of those LDGs, however, depended on the scale and metric used to describe diversity. It is proposed that patterns of LDGs at various scales are not the result of a single overarching process but are strongly influenced by local and regional processes. Although the most evident environmental gradient was the decrease in SST towards the south, it was demonstrated that regional and local environmental variables were also important for understanding the increase in regional β‐diversity towards the tropics.
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