Coral and Seawater Metagenomes Reveal Key Microbial Functions to Coral Health and Ecosystem Functioning Shaped at Reef Scale

Abstract

The coral holobiont is comprised of a highly diverse microbial community that provides key services to corals such as protection against pathogens and nutrient cycling. The coral surface mucus layer (SML) microbiome is very sensitive to external changes, as it constitutes the direct interface between the coral host and the environment. Here, we investigate whether the bacterial taxonomic and functional profiles in the coral SML are shaped by the local reef zone and explore their role in coral health and ecosystem functioning. The analysis was conducted using metagenomes and metagenome-assembled genomes (MAGs) associated with the coral Pseudodiploria strigosa and the water column from two naturally distinct reef environments in Bermuda: inner patch reefs exposed to a fluctuating thermal regime and the more stable outer reefs. The microbial community structure in the coral SML varied according to the local environment, both at taxonomic and functional levels. The coral SML microbiome from inner reefs provides more gene functions that are involved in nutrient cycling (e.g., photosynthesis, phosphorus metabolism, sulfur assimilation) and those that are related to higher levels of microbial activity, competition, and stress response. In contrast, the coral SML microbiome from outer reefs contained genes indicative of a carbohydrate-rich mucus composition found in corals exposed to less stressful temperatures and showed high proportions of microbial gene functions that play a potential role in coral disease, such as degradation of lignin-derived compounds and sulfur oxidation. The fluctuating environment in the inner patch reefs of Bermuda could be driving a more beneficial coral SML microbiome, potentially increasing holobiont resilience to environmental changes and disease.

Heat-stressed coral microbiomes are stable and potentially beneficial at the level of taxa and functional genes

“…Therefore, we selected this period to capture a potential long-term acclimatization of the coral holobiont to their reef zones, and not their immediate response to acute temperature fluctuations. The mucus from P. strigosa was collected from six colonies from the inner and outer reef zones (n = 12 colonies total) to describe the natural spatial variability in the coral microbiome (Lima et al 2020(Lima et al , 2022. After the mucus sampling, each coral colony was collected using a hammer and chisel to be used in the experiments to assess heat resistance.…”

“…Productivity and respiration rates and photochemical efficiency were measured the day before the heat treatment started (post-acclimation or pre-treatment) and on day 6, which is the final day of the experiment (post-treatment). The coral mucus was collected at the end of each incubation for respirometry using a two-way 50 ml syringe that is filled with 0.02 μm filtered seawater (Lima et al 2020(Lima et al , 2022. The filtered seawater is flowed across the coral surface, dislodging the mucus and associated microbes, which are then sucked up via the recirculating tube, and resulting sample pushed through a 0.22 μm sterivex for DNA extraction.…”

“…Metagenomes were sequenced from a subset of the coral nubbins used in the experiment (n = 8), representing four different coral colonies (n = 2 colonies per reef zone) that had their mucus sampled before and after the experimental treatments (n = 16 metagenomes total). These metagenomes were compared with the ones from the same colonies collected in situ (Lima et al 2022).…”

“…The coral holobiont depends on key services such as nitrogen and sulfur cycling mediated by the associated microbiome (Wegley et al 2007;Siboni et al 2008;Raina et al 2013;Rädecker et al 2015). The coral surface mucous layer (SML) sustains a diverse and abundant community of these microbial partners (Koren and Rosenberg 2006;Sharon and Rosenberg 2008;Garren and Azam 2012;Ainsworth et al 2015;Lima et al 2020Lima et al , 2022. The coral microbiome benefits from the high nitrogen content and organic matter in the SML (Wild et al 2005;Rädecker et al 2015) and provides protection against coral pathogens via production of antimicrobials (Ritchie 2006;Krediet et al 2013).…”

Microbial Community Diversity of Coral Reef Sediments on Liuqiu Island, Southwestern Taiwan

“…Tropical coral reefs are highly diverse ecosystems in which complex environments provide diverse habitats and niches over time and space [1,2]. Microbial communities, including bacteria, microbial eukaryotes (fungi), and small eukaryotes, play an important role in nutrient cycling in coral reef ecosystems, encompassing many pelagic and benthic processes [3][4][5][6][7][8]. Vertical community stratification caused by redox gradients enables highly diverse microbial communities in coral reef sediments [9].…”