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Bacterial ASVs representative of host genotype and reef habitat. Indicator bacterial ASVs associated with contribution of host genotype (A, B) and environment (C, D) to bacterial community structure. Heatmap based on IndicSpecies analysis shows specific bacterial ASVs that characterize (A) each host genotype, numbered from G1 to G6 and (C) fire corals in each of the three habitats, mid slope (MD), upper slope (UP), and back reef (BR). Each cell represents the standard transformation of the counts for each specific ASVs per genotype and habitat. B Specific bacterial families associated with host genotype and (D) reef habitat. Bar plots represent the relative abundance of the counts for each identified specific bacterial ASV at the family level, represented by a unique color; less common specific bacterial families were grouped as ‘Other specific bacteria’ and are shown in light gray; dotted bars are ASVs that are not specific to one of the six genotypes and to one of the three habitats, note different scales in B and D. See Supplementary Data 4 for details on IndicSpecies analysis.
Source publication
Coral microbiomes are critical to holobiont functioning, but much remains to be understood about how prevailing environment and host genotype affect microbial communities in ecosystems. Resembling human identical twin studies, we examined bacterial community differences of naturally occurring fire coral clones within and between contrasting reef ha...
Citations
... Interestingly, the coral colonies tested here maintained distinct bacterial microbiomes even after longterm co-culturing, which supports a degree of host genotype effects controlling the microbiome composition, as previously reported from Hydrozoan and other coral species in the field (Pollock et al. 2018;Dubé et al. 2021). Surprisingly, the microbiome of one Red Sea colony was highly similar to that of Hong Kong colonies. ...
... This appears counterintuitive as colonies from the Red Sea and Hong Kong may belong to different Galaxea lineages (sensu Wepfer et al. 2020), and considering the large differences in environmental conditions at their origin. While these colonies were also maintained in separate facilities, rearing conditions were similar at both locations (i.e., temperature, salinity, illumination) and may have induced convergence of microbial community composition (Dubé et al. 2021). On the other hand, G. fascicularis is a polyphyletic species that contains several morphologically cryptic lineages (Wepfer et al. 2020) and the dissimilarity between colonies from the Red Sea could reflect host phylogentic differences (i.e., cryptic species within the same region). ...
... The compositions of coral microbiomes can vary substantially between and within coral species and across geographic locations [20,37,38]. The genotype of the host coral underlies some of this variation [37,39,40], as do environmental factors such as water temperature [41], habitat type [42], and pollution levels [41,43]. ...
... The compositions of coral microbiomes can vary substantially between and within coral species and across geographic locations [20,37,38]. The genotype of the host coral underlies some of this variation [37,39,40], as do environmental factors such as water temperature [41], habitat type [42], and pollution levels [41,43]. These factors can differ across the ranges of coral species, yet the scope of most studies is limited to a narrow selection of a species' known geographic or depth range. ...
Background
Coral-associated microbiomes vary greatly between colonies and localities with functional consequences on the host. However, the full extent of variability across the ranges of most coral species remains unknown, especially for corals living in deep waters which span greater ranges. Here, we characterized the microbiomes of four octocoral species from mesophotic and bathyal deep-sea habitats in the northern Gulf of Mexico, Muricea pendula, Swiftia exserta, Callogorgia delta, and Paramuricea biscaya, using 16S rRNA gene metabarcoding. We sampled extensively across their ranges to test for microbiome differentiation between and within species, examining the influence of environmental factors that vary with depth (53–2224 m) and geographic location (over 680 m) as well as the host coral’s genotype using RAD-sequencing.
Results
Coral microbiomes were often dominated by amplicon sequence variants whose abundances varied across their hosts’ ranges, including symbiotic taxa: corallicolids, Endozoicomonas , members of the Mollicutes , and the BD1-7 clade. Coral species, depth, and geographic location significantly affected diversity, microbial community composition, and the relative abundance of individual microbes. Depth was the strongest environmental factor determining microbiome structure within species, which influenced the abundance of most dominant symbiotic taxa. Differences in host genotype, bottom temperature, and surface primary productivity could explain a significant part of the microbiome variation associated with depth and geographic location.
Conclusions
Altogether, this work demonstrates that the microbiomes of corals in deep waters vary substantially across their ranges in accordance with depth and other environmental conditions. It reveals that the influence of depth on the ecology of mesophotic and deep-sea corals extends to its effects on their microbiomes which may have functional consequences. This work also identifies the distributions of microbes including potential parasites which can be used to inform restoration plans in response to the Deepwater Horizon oil spill.
... Similarity percentage difference contribution analysis was performed using the "simper" function in the "vegan" package to quantify the contribution of each species to the difference between the two groups. Overall variability between groups was calculated using ANOSIM [48]. Linear discriminant analysis (LDA) effect size (LEfSe) analysis was also conducted [49]. ...
Winter supplemental feeding (SF) is commonly used to improve the survival of captive wildlife. To investigate the impact of winter supplementation on the gut microbiota of wildlife, we assessed changes in the gut microbiota of red deer (Cervus elaphus) during the supplementary and non-supplementary feeding (NSF) groups using 16S rRNA sequencing technology. We found no significant differences in the diversity of the gut microbiota between SF and NSF except for the Simpson’s index. However, the relative abundance of Bacteroidetes, Lentisphaerae, and Proteobacteria in the gut microbiota was significantly higher during SF. Further, genera such as Intestinimonas, Rikenella, Lawsonibacter, Muribaculum, and Papillibacter were more abundant during SF. Beta diversity analysis showed significant differences between SF and NSF. The microbes detected during SF were primarily associated with lipid metabolism, whereas those detected during NSF were linked to fiber catabolism. High-energy feed affects the gut microbial composition and function in red deer. During SF, the gut microbes in red deer were enriched in microorganisms associated with butyrate and lipid metabolism, such as R. microfusus, M. intestinale, and Papillibacter cinnamivorans. These gut microbes may be involved in ameliorating obesity associated with high-energy diets. In summary, SF is a reasonable and effective management strategy.
... Despite recent advances, the mechanisms by which bacteria from the coral microbiome exert specific functions are largely unknown (Table 1). An ongoing debate in microbiome research addresses to what extent taxonomy is indicative of function and whether useful measures can be derived from comparing taxonomy with function (for example, diversity, stability or health) 46,146 . Although the promise of microbiome manipulation to increase coral performance has been shown in principle, it is unclear whether it is applicable broadly across species. ...
Stony corals, the engines and engineers of reef ecosystems, face unprecedented threats from anthropogenic environmental change. Corals are holobionts that comprise the cnidarian animal host and
a diverse community of bacteria, archaea, viruses and eukaryotic microorganisms. Recent research shows that the bacterial microbiome has a pivotal role in coral biology. A healthy bacterial assemblage contributes to nutrient cycling and stress resilience, but pollution, overfishing and climate change can break down these symbiotic relationships, which results in disease, bleaching and, ultimately,
coral death. Although progress has been made in characterizing
the spatial-temporal diversity of bacteria, we are only beginning to appreciate their functional contribution. In this Review, we summarize the ecological and metabolic interactions between bacteria and other holobiont members, highlight the biotic and abiotic factors influencing the structure of bacterial communities and discuss the impact of climate change on these communities and their coral hosts. We emphasize how microbiome-based interventions can
help to decipher key mechanisms underpinning coral health and promote reef resilience. Finally, we explore how recent technological developments may be harnessed to address some of the most pressing challenges in coral microbiology, providing a road map for future research in this field.
... This is in line with observations that PMA treatment increases evenness and diversity without a change in the number of ASVs, a phenomenon driven by increased detection of rare taxa [30,31,98]. We also found that that coral microbiota varied by genotype for A. kenti, P. daedalea, and P. lutea, which has previously been reported [78,87,99]. ...
Background
Nucleic acid-based analytical methods have greatly expanded our understanding of global prokaryotic diversity, yet standard metabarcoding methods provide no information on the most fundamental physiological state of bacteria, viability. Scleractinian corals harbour a complex microbiome in which bacterial symbionts play critical roles in maintaining health and functioning of the holobiont. However, the coral holobiont contains both dead and living bacteria. The former can be the result of corals feeding on bacteria, rapid swings from hyper- to hypoxic conditions in the coral tissue, the presence of antimicrobial compounds in coral mucus, and an abundance of lytic bacteriophages.
Results
By combining propidium monoazide (PMA) treatment with high-throughput sequencing on six coral species (Acropora loripes, A. millepora, A. kenti, Platygyra daedalea, Pocillopora acuta, and Porites lutea) we were able to obtain information on bacterial communities with little noise from non-viable microbial DNA. Metabarcoding of the 16S rRNA gene showed significantly higher community evenness (85%) and species diversity (31%) in untreated compared with PMA-treated tissue for A. loripes only. While PMA-treated coral did not differ significantly from untreated samples in terms of observed number of ASVs, > 30% of ASVs were identified in untreated samples only, suggesting that they originated from cell-free/non-viable DNA. Further, the bacterial community structure was significantly different between PMA-treated and untreated samples for A. loripes and P. acuta indicating that DNA from non-viable microbes can bias community composition data in coral species with low bacterial diversity.
Conclusions
Our study is highly relevant to microbiome studies on coral and other host organisms as it delivers a solution to excluding non-viable DNA in a complex community. These results provide novel insights into the dynamic nature of host-associated microbiomes and underline the importance of applying versatile tools in the analysis of metabarcoding or next-generation sequencing data sets.
Supplementary Information
The online version contains supplementary material available at 10.1186/s40793-023-00541-6.
... Characterized by digitated growth forms (Figure 6), Acropora branches break relatively easily into loose fragments that show a high capacity to survive and reattach to the substrate [12]. Similarly, Galaxea colonies often split into detached individual polyps (Figure 7), and Millepora pieces into free branches and columns that are dispersed by waves [32]. Nevertheless, recent investigations in our study system indicate that the outer reef receives lower rates of larval settlement than nearby lagoon sites, and that several coral taxa exhibit lower competitive performances there as compared to other reef environments [25,31]. ...
... Characterized by digitated growth forms ( Figure 6), Acropora branches break relatively easily into loose fragments that show a high capacity to survive and reattach to the substrate [12]. Similarly, Galaxea colonies often split into detached individual polyps (Figure 7), and Millepora pieces into free branches and columns that are dispersed by waves [32]. Nevertheless, recent investigations in our study system indicate that the outer reef receives lower rates of larval settlement than nearby lagoon sites, and that several coral taxa exhibit lower competitive performances there as compared to other reef environments [25,31]. ...
Demographic studies that quantify species’ performances for survival, growth, and reproduction are powerful means to characterize sources of demographic bottlenecks and predict community dynamics. However, they require fine-scale surveys of populations in the field, and are often too effort-intensive to be replicable at a large scale and in the long term. We developed a standardized digital approach for extracting demographic data on species’ abundances, sizes, and positions within video transects, enabling back-from-the-field data acquisition and therefore optimizing time spent in the field. The approach is based on manual species identification, size measurements, and mapping in video transects, mimicking what is traditionally performed in the field, though it can be automated in the future with the deployment of artificial intelligence. We illustrate our approach using video surveys of a reef-building coral community in New Caledonia. The results characterize the composition of the coral community and demographic performances as key ecological indicators of coral reef health, shed light on species’ life strategies and constraints to their demographics, and open paths for further quantitative investigations. Key findings include the diversity of life strategies with contrasting levels of investment in survival, growth, and reproduction found among the six taxa dominating the coral community (Acropora, Montipora, Porites, Galaxea, Favia, Millepora), indicating the diversity of demographic paths to ecological success. Our results also indicate that several species have adapted mechanisms to prevail under limiting hydrodynamic environments through the propagation of coral fragments. Our approach facilitates image-based demographic investigations, supporting endeavors in ecology and ecosystem management.
... This focus has framed our current understanding of cnidarian microbiomes. Research into non-scleractinian cnidarians, however, has identified significantly different structuring of cnidarian microbial symbioses [34][35][36] . Unfortunately, the lack of standardized sampling, storage, processing, and analytical protocols across 16S rRNA gene amplicon studies, hinders the ability to synthesize published data to create a baseline for cnidarian microbiomes [37][38][39] . ...
Microorganisms play essential roles in the health and resilience of cnidarians. Understanding the factors influencing cnidarian microbiomes requires cross study comparisons, yet the plethora of protocols used hampers dataset integration. We unify 16S rRNA gene sequences from cnidarian microbiome studies under a single analysis pipeline. We reprocess 12,010 cnidarian microbiome samples from 186 studies, alongside 3,388 poriferan, 370 seawater samples, and 245 cultured Symbiodiniaceae, unifying ~6.5 billion sequence reads. Samples are partitioned by hypervariable region and sequencing platform to reduce sequencing variability. This systematic review uncovers an incredible diversity of 86 archaeal and bacterial phyla associated with Cnidaria, and highlights key bacteria hosted across host sub-phylum, depth, and microhabitat. Shallow (< 30 m) water Alcyonacea and Actinaria are characterized by highly shared and relatively abundant microbial communities, unlike Scleractinia and most deeper cnidarians. Utilizing the V4 region, we find that cnidarian microbial composition, richness, diversity, and structure are primarily influenced by host phylogeny, sampling depth, and ocean body, followed by microhabitat and sampling date. We identify host and geographical generalist and specific Endozoicomonas clades within Cnidaria and Porifera. This systematic review forms a framework for understanding factors governing cnidarian microbiomes and creates a baseline for assessing stress associated dysbiosis.
... iron sequestration and oxygen stress response) and this response has been found to have intraspecific variability and related to how genetically similar the coral colonies are (Parkinson et al., 2015). Multiple other recent examples in corals have also demonstrated the influence of host genotype on the associated microbial communities (Acropora tenuis, Glasl et al., 2019; and Millepora sp., Dubé et al., 2021). Similarly, a higher genetic relatedness among sponges of the same species has been seen to translate into a higher similarity of their associated microbiome (Griffiths et al., 2019). ...
A fundamental question in holobiont biology is the extent to which microbiomes are determined by host characteristics regulated by their genotype. Studies on the interactions of host genotype and microbiomes are emerging but disentangling the role that host genotype has in shaping microbiomes remains challenging in natural settings. Host genotypes tend to be segregated in space and affected by different environments. Here we overcome this challenge by studying an unusual situation where host asexual (5 clonal lineages) and sexual genotypes (15 non-clonal lineages) of the same species co-occur under the same environment. This allowed us to partition the influence of morphological traits and genotype in shaping host-associated bacterial communities. Lamina-associated bacteria of co-occurring kelp sexual non-clonal (Ecklonia radiata) and asexual clonal (E. brevipes) morphs were compared to test whether host genotype influences microbiomes beyond morphology. Similarity of bacterial composition and predicted functions were evaluated among individuals within a single clonal genotype or among non-clonal genotypes of each morph. Higher similarity in bacterial composition and inferred functions were found among identical clones of E. brevipes compared to other clonal genotypes or unique non-clonal E. radiata genotypes. Additionally, bacterial diversity and composition differed significantly between the two morphs and were related with one morphological trait in E. brevipes (haptera). Thus, factors regulated by the host genotype (e.g. secondary metabolite production) likely drive differences in microbial communities between morphs. The strong association of genotype and microbiome found here highlights the importance of genetic relatedness of hosts in determining variability in their bacterial symbionts.
... The fact that morphotype differences in microbial community composition were large, and that the explanatory power of site was relatively higher than the explanatory power of the environmental conditions, suggests that the host itself may be the main structuring factor. A recent study on clonal Millepora colonies showed that microbial communities that differed between host genotype, within habitats, were potentially functionally redundant 52 . Observed differences in microbial communities may thus mask similar functional profiles of functionally redundant microbiomes 53 . ...
Coral reefs are among the most diverse ecosystems on Earth. They support high biodiversity of multicellular organisms that strongly rely on associated microorganisms for health and nutrition. However, the extent of the coral reef microbiome diversity and its distribution at the oceanic basin-scale remains to be explored. Here, we systematically sampled 3 coral morphotypes, 2 fish species, and planktonic communities in 99 reefs from 32 islands across the Pacific Ocean, to assess reef microbiome composition and biogeography. We show a very large richness of reef microorganisms compared to other environments, which extrapolated to all fishes and corals of the Pacific, approximates the current estimated total prokaryotic diversity for the entire Earth. Microbial communities vary among and within the 3 animal biomes (coral, fish, plankton), and geographically. For corals, the cross-ocean patterns of diversity are different from those known for other multicellular organisms. Within each coral morphotype, community composition is always determined by geographic distance first, both at the island and across ocean scale, and then by environment. Our unprecedented sampling effort of coral reef microbiomes, as part of the Tara Pacific expedition, provides new insight into the global microbial diversity, the factors driving their distribution, and the biocomplexity of reef ecosystems.
... The question of host-specificity remains open, however, since some Endozoicomonadaceae types could be shared between different hosts 41 , different Endozoicomonadaceae types can dominate within a same host 43 , and changes in their relative abundance seems to be independent of the symbiotic algae 46 . If the host is not the driver of microbiome composition, external factors could play a role 47 . Endozoicomonadaceae communities could be shaped by environmental factors as they were shown to be less abundant in Acropora millepora at lower seawater pH 48,49 , or during increased temperatures and subsequent bleaching 31,50 , as well as anthropogenic impact and habitat suitability 44,51 . ...
Health and resilience of the coral holobiont depend on diverse bacterial communities often dominated by key marine symbionts of the Endozoicomonadaceae family. The factors controlling their distribution and their functional diversity remain, however, poorly known. Here, we study the ecology of Endozoicomonadaceae at an ocean basin-scale by sampling specimens from three coral genera (Pocillopora, Porites, Millepora) on 99 reefs from 32 islands across the Pacific Ocean. The analysis of 2447 metabarcoding and 270 metagenomic samples reveals that each coral genus harbored a distinct new species of Endozoicomonadaceae. These species are composed of nine lineages that have distinct biogeographic patterns. The most common one, found in Pocillopora, appears to be a globally distributed symbiont with distinct metabolic capabilities, including the synthesis of amino acids and vitamins not produced by the host. The other lineages are structured partly by the host genetic lineage in Pocillopora and mainly by the geographic location in Porites. Millepora is more rarely associated to Endozoicomonadaceae. Our results show that different coral genera exhibit distinct strategies of host-Endozoicomonadaceae associations that are defined at the bacteria lineage level.
