Microbial ecology of coral-dominated reefs in the Federated States of Micronesia

Abstract

Microorganisms are central to the functioning of coral reef ecosystems, but their dynamics are unstudied on most reefs. We examined the microbial ecology of shallow reefs within the Federated States of Micronesia. We surveyed 20 reefs surrounding 7 islands and atolls (Yap, Woleai, Olimarao, Kosrae, Kapingamarangi, Nukuoro, and Pohnpei), spanning 875053 km2. On the reefs, we found consistently higher coral coverage (mean ± SD = 36.9 ± 22.2%; max 77%) compared to macroalgae coverage (15.2 ± 15.5%; max 58%), and low abundances of fish. Reef waters had low inorganic nutrient concentrations and were dominated by Synechococcus, Prochlorococcus, and SAR11 bacteria. The richness of bacterial and archaeal communities was significantly related to interactions between island/atoll and depth. High coral coverage on reefs was linked to higher relative abundances of Flavobacteriaceae, Leisingera, Owenweeksia, Vibrio, and the OM27 clade, as well as other heterotrophic bacterial groups, consistent with communities residing in waters near corals and within coral mucus. Microbial community structure at reef depth was significantly correlated with geographic distance, suggesting that island biogeography influences reef microbial communities. Reefs at Kosrae Island, which hosted the highest coral abundance and diversity, were unique compared to other locations; seawater from Kosrae reefs had the lowest organic carbon (59.8-67.9 µM), highest organic nitrogen (4.5-5.3 µM), and harbored consistent microbial communities (>85% similar), which were dominated by heterotrophic cells. This study suggests that the reef-water microbial ecology on Micronesian reefs is influenced by the density and diversity of corals as well as other biogeographical features.

Microbial Interactions with Dissolved Organic Matter Are Central to Coral Reef Ecosystem Function and Resilience

“…The role of DOM in controlling the composition of microbial communities may be a key part of nutrient retention and recycling, ultimately controlling the persistence of reefs. Consistent patterns of reef-associated microbial taxa have emerged, including a set that are significantly enriched in reef habitats across the Pacific (Rhodobacteraceae, Sphingomonadaceae, Flavobacteriaceae, Moraxellaceae, Hyphomonadaceae, Methylophagaceae, Vibrionaceae, and Rhizobiaceae; Table 1) and additional taxa that are consistently associated with reefs worldwide (Alteromonadaceae, Halomonadaceae, and Cryomorphaceae; e.g., Apprill et al 2021, Frade et al 2020, Weber et al 2019, Wegley Kelly et al 2014; Table 1). Many of these taxa likely play key roles in microbially mediated nutrient transformations.…”

“…Broad surveys have defined some microbial groups that are enriched on reefs relative to the ocean. Table 1 links paired coral reef benthos-water column survey data from 54 coral reef sites throughout 22 islands across the insular North Pacific to compiled literature data comparing reef-associated microbial taxa with those of the associated oceanic regime, resolving broad taxonomic groupings that are consistently enriched on reefs in the Great Barrier Reef (Frade et al 2020, Tout et al 2014, the Caribbean (Weber & Apprill 2020;Weber et al 2019Weber et al , 2020b, and the Pacific (Apprill et al 2021, Wegley Kelly et al 2014. Offshore oceanic communities are dominated by Cyanobiaceae (Prochlorococcus and Synechococcus), the Gammaproteobacteria SAR86, Actinomarinaceae, and the Alphaproteobacteria families Pelagibacteraceae (SAR11) and Puniceispirillaceae (SAR116), while nearshore communities are enriched with Rhodobacteraceae, Sphingomonadaceae, Flavobacteriaceae, and Alteromonadaceae; these groups and others highlighted in Table 1 are candidates for further exploration of the types of organisms that may play central roles in the function of reef ecosystems.…”

Microorganisms uniquely capture and predict stony coral tissue loss disease and hurricane disturbance impacts on US Virgin Island reefs

“…In contrast to this, as ammonium increased we noted enrichment of the oligotrophic heterotrophs SAR11 and SAR86, which were some of the most abundant microorganisms in our dataset (Dupont et al, 2012; Lauro et al, 2009). These microorganisms are common in reef water and grow in response to coral and CCA exudates (Apprill et al, 2021; McNally et al, 2017; Nelson et al, 2023; Quinlan et al, 2019). Our heterotrophic microbial abundance analysis captured heterotrophs from both oligotrophic and copiotrophic life strategies, and we additionally measured total organic carbon (TOC).…”

“…Microorganisms in reef water show promise as targets for revealing reef ecosystem changes because of their ability to respond to gradients in environmental conditions (Glasl et al, 2017(Glasl et al, , 2018. Reef water microorganisms are responsive to changes in coral and algal cover across different reefs (Apprill et al, 2021;Glasl et al, 2019;Haas et al, 2016). They are also structured by yearly temperature patterns and driven by seasonality (Glasl et al, 2019(Glasl et al, , 2020.…”

Toward a New Era of Coral Reef Monitoring

“…Given the fast rate of microbial growth and organismal-based metabolite production and consumption on reefs, microbial and/or metabolite profiles in reef water can provide non-invasive, temporally sensitive measures of reef and environmental conditions. Observations of reef water microbial communities capture microbial processes on reefs, which are often linked to water quality, macro-organismal composition, protection and conservation status, oceanographic and biogeographic patterns, − and even pathogens . Additionally, reef organisms excrete distinct metabolites into reef waters, which contribute to reef biogeochemistry and microbial processes, − coral heat stress, and cues for recruitment and predation processes. , Reef water also contains environmental DNA (e.g., eDNA) from eukaryotic organisms, including fish and other mobile organisms, and eDNA provides insights into reef biodiversity and community patterns. , To capture eDNA as well as microbial and metabolite patterns on reefs, discrete volumes of water are collected by divers using Niskin bottles or syringes or vessel-based sampling devices.…”