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Abstract Coral bleaching events from thermal stress are increasing globally in duration, frequency, and intensity. While bleaching can cause mortality, some corals survive, reacquire symbionts, and recover. We experimentally bleachedMontipora capitatato examine molecular and physiological differences between corals that recover (resilient) and those that die (susceptible). Corals were collected and monitored for eight months post-bleaching to identify genets with long-term resilience. Using an integrated systems-biology approach that included quantitative proteomics, 16S rRNA sequencing to characterize the coral microbiome, total coral lipids, symbiont community composition and density, we explored molecular-level mechanisms of tolerance in corals pre- and post-bleaching. Prior to thermal stress, resilient corals have a more diverse microbiome and abundant proteins essential for carbon acquisition, symbiont retention, and pathogen resistance. Protein signatures of susceptible corals showed early symbiont rejection and utilized urea for carbon and nitrogen. Our results reveal molecular factors for surviving bleaching events and identify diagnostic protein biomarkers for reef management and restoration. 

Abstract The genomes of mitochondria and chloroplasts contain ribosomal RNA (rRNA) genes, reflecting their ancestry as free-living bacteria. These organellar rRNAs are often amplified in microbiome studies of animals and plants. If identified, they can be discarded, merely reducing sequencing depth. However, we identify certain high-abundance organeller RNAs not identified by common pipelines, which may compromise statistical analysis of microbiome structure and diversity. We quantified this by reanalyzing 7459 samples from seven 16S rRNA studies, including microbiomes from 927 unique animal genera. We find that under-annotation of cryptic mitochondrial and chloroplast reads affects multiple of these large-scale cross-species microbiome comparisons, and varies between host species, biasing comparisons. We offer a straightforward solution: supplementing existing taxonomies with diverse organelle rRNA sequences. This resolves up to 97% of unique unclassified sequences in some entire studies as mitochondrial (14% averaged across all studies), without increasing false positive annotations in mitochondria-free mock communities. Improved annotation decreases the proportion of unknown sequences by ≥10-fold in 2262 of 7459 samples (30%), spanning five of seven major studies examined. We recommend leveraging organelle sequence diversity to better identify organelle gene sequences in microbiome studies, and provide code, data resources and tutorials that implement this approach. 

Background Evolutionary tradeoffs between life-history strategies are important in animal evolution. Because microbes can influence multiple aspects of host physiology, including growth rate and susceptibility to disease or stress, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a biodiverse, data-rich, and ecologically-relevant host system to explore this idea. Results Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by conducting a cross-species coral microbiome survey (the “Global Coral Microbiome Project”) and combining the results with long-term global disease prevalence and coral trait data. Interpreting these data in their phylogenetic context, we show that microbial dominance predicts disease susceptibility, and traced this dominance-disease association to a single putatively beneficial symbiont genus, Endozoicomonas. Endozoicomonas relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera, while also correlating strongly with high growth rates. Conclusions These results demonstrate that the evolution ofEndozoicomonassymbiosis in corals correlates with both disease prevalence and growth rate, and suggest a mediating role. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbioses influence animal life-history tradeoffs. 

As climate change drives health declines of tropical reef species, diseases are further eroding ecosystem function and habitat resilience. Coral disease impacts many areas around the world, removing some foundation species to recorded low levels and thwarting worldwide efforts to restore reefs. What we know about coral disease processes remains insufficient to overcome many current challenges in reef conservation, yet cumulative research and management practices are revealing new disease agents (including bacteria, viruses, and eukaryotes), genetic host disease resistance factors, and innovative methods to prevent and mitigate epizootic events (probiotics, antibiotics, and disease resistance breeding programs). The recent outbreak of stony coral tissue loss disease across the Caribbean has reenergized and mobilized the research community to think bigger and do more. This review therefore focuses largely on novel emerging insights into the causes and mechanisms of coral disease and their applications to coral restoration and conservation. 

Despite advances in sequencing, lack of standardization makes comparisons across studies challenging and hampers insights into the structure and function of microbial communities across multiple habitats on a planetary scale. Here we present a multi-omics analysis of a diverse set of 880 microbial community samples collected for the Earth Microbiome Project. We include amplicon (16S, 18S, ITS) and shotgun metagenomic sequence data, and untargeted metabolomics data (liquid chromatography-tandem mass spectrometry and gas chromatography mass spectrometry). We used standardized protocols and analytical methods to characterize microbial communities, focusing on relationships and co-occurrences of microbially related metabolites and microbial taxa across environments, thus allowing us to explore diversity at extraordinary scale. In addition to a reference database for metagenomic and metabolomic data, we provide a framework for incorporating additional studies, enabling the expansion of existing knowledge in the form of an evolving community resource. We demonstrate the utility of this database by testing the hypothesis that every microbe and metabolite is everywhere but the environment selects. Our results show that metabolite diversity exhibits turnover and nestedness related to both microbial communities and the environment, whereas the relative abundances of microbially related metabolites vary and co-occur with specific microbial consortia in a habitat-specific manner. We additionally show the power of certain chemistry, in particular terpenoids, in distinguishing Earth’s environments (for example, terrestrial plant surfaces and soils, freshwater and marine animal stool), as well as that of certain microbes including Conexibacter woesei (terrestrial soils), Haloquadratum walsbyi (marine deposits) and Pantoea dispersa (terrestrial plant detritus). This Resource provides insight into the taxa and metabolites within microbial communities from diverse habitats across Earth, informing both microbial and chemical ecology, and provides a foundation and methods for multi-omics microbiome studies of hosts and the environment. 

Coevolution—reciprocal evolutionary change between interacting lineages (Thompson, 1994; see Glossary)—is thought to have played a profound role in the evolution of Life on Earth. From similar patterns across the wings of unrelated lineages of butterflies (Hoyal Cuthill and Charleston, 2015), egg mimicry of “cheating” brood parasites (Davies, 2010), to the role of animal pollinators in driving the diversification of flowering plants (Kay and Sargent, 2009), to the ubiquity of sexual reproduction and sexual conflicts (Hamilton, 2002; Arnqvist and Rowe, 2005; King et al., 2009), the formation of the eukaryotic cell (Martin et al., 2015; Imachi et al., 2020), and even the origin of living organisms themselves (Mizuuchi and Ichihashi, 2018), evolutionary changes among interacting lineages have played profound and important roles in the history of Life. This Grand Challenges inaugural contribution encompasses eclectic opinions of the editorial board as to what are the next frontiers of coevolution research in the 21st century. Coevolutionary biology is a field that has garnered a lot of attention in recent years, in part as a result of technical advances in nucleotide sequencing and bioinformatics in the burgeoning field of host–microbial interactions. Many seminal studies of coevolution examined reciprocal evolutionary change between two or a few interacting macroscopic species that imposed selective pressures on one another (e.g., insect or bird pollinators and their flowering host plants). Understanding the contexts under which coevolution occurs, as opposed to scenarios in which each partner adapts independently to a particular environment (Darwin, 1862; Stiles, 1978) is important to elucidate coevolutionary processes. A whole spectrum of organismal interactions has been examined under the lens of coevolution, providing additional context, and nuance to ecological strategies traditionally categorized as ranging from beneficial to detrimental for participating species (Figure 1). In particular, a coevolutionary perspective has revealed that even “mutualisms” are not always fully beneficial or cooperative for the partners involved. Instead, the tendency to “cheat” permeates across symbiotic partnerships (Perez-Lamarque et al., 2020). Conversely, recent evidence suggests that non-lethal predation by co-evolved predators, which has traditionally been assumed to be entirely antagonistic, may provide sessile prey with some indirect benefit through enhanced opportunities to acquire beneficial symbiotic microorganisms (Grupstra et al., 2021). Herein, we discuss some of the recent areas of active research in coevolution, restricting our focus to coevolution between interacting species. 

Coral diseases have increased in frequency and intensity around the tropics worldwide. However, in many cases, little is known about their etiology. Montipora white syndrome (MWS) is a common disease affecting the coral Montipora capitata, a major reef builder in Hawai'i. Chronic Montipora white syndrome (cMWS) is a slow- moving form of the disease that affects M. capitata throughout the year. The effects of this chronic disease on coral immunology and microbiology are currently unknown. In this study, we use prophenoloxidase immune assays and 16S rRNA gene amplicon sequencing to characterize the microbiome and immunological response associated with cMWS. Our results show that immunological and microbiological responses are highly localized. Relative to diseased samples, apparently healthy portions of cMWS corals differed in immune activity and in the relative abundance of microbial taxa. Coral tissues with cMWS showed decreased tyrosinase- type catecholase and tyrosinase- type cresolase activity and increased laccase- type activity. Catecholase and cresolase activity were negatively correlated across all tissue types with microbiome richness. The localized effect of cMWS on coral microbiology and immunology is probably an important reason for the slow progression of the disease. This local confinement may facilitate interventions that focus on localized treatments on tissue types. This study provides an important baseline to understand the interplay between the microbiome and immune system and the mechanisms used by corals to manage chronic microbial perturbations associated with white syndrome. 

Coral diseases have increased in frequency and intensity around the tropics worldwide. However, in many cases, little is known about their etiology. Montipora white syndrome (MWS) is a common disease affecting the coral Montipora capitata, a major reef builder in Hawai'i. Chronic Montipora white syndrome (cMWS) is a slow-moving form of the disease that affects M. capitata throughout the year. The effects of this chronic disease on coral immunology and microbiology are currently unknown. In this study, we use prophenoloxidase immune assays and 16S rRNA gene amplicon sequencing to characterize the microbiome and immunological response associated with cMWS. Our results show that immunological and microbiological responses are highly localized. Relative to diseased samples, apparently healthy portions of cMWS corals differed in immune activity and in the relative abundance of microbial taxa. Coral tissues with cMWS showed decreased tyrosinase-type catecholase and tyrosinase-type cresolase activity and increased laccase-type activity. Catecholase and cresolase activity were negatively correlated across all tissue types with microbiome richness. The localized effect of cMWS on coral microbiology and immunology is probably an important reason for the slow progression of the disease. This local confinement may facilitate interventions that focus on localized treatments on tissue types. This study provides an important baseline to understand the interplay between the microbiome and immune system and the mechanisms used by corals to manage chronic microbial perturbations associated with white syndrome. 

The microbiomes of tropical corals are actively studied using 16S rRNA gene amplicons to understand microbial roles in coral health, metabolism, and disease resistance. However, primers targeting bacterial and archaeal 16S rRNA genes may also amplify organelle rRNA genes from the coral, associated microbial eukaryotes, and encrusting organisms. In this manuscript, we demonstrate that standard workflows for annotating microbial taxonomy severely under-annotate mitochondrial sequences in 1272 coral microbiomes from the Earth Microbiome Project. This issue prevents annotation of >95% of reads in some samples and persists when using either Greengenes or SILVA taxonomies. Worse, mitochondrial under-annotation varies between species and across anatomy, biasing comparisons of α- and β-diversity. By supplementing existing taxonomies with diverse mitochondrial rRNA sequences, we resolve ~97% of unique unclassified sequences as mitochondrial, without increasing misannotation in mock communities. We recommend using these extended taxonomies for coral microbiome analysis and encourage vigilance regarding similar issues in other hosts.