Thermal Stress Interacts With Surgeonfish Feces to Increase Coral Susceptibility to Dysbiosis and Reduce Tissue Regeneration

Abstract

Dysbiosis of coral microbiomes results from various biotic and environmental stressors, including interactions with important reef fishes which may act as vectors of opportunistic microbes via deposition of fecal material. Additionally, elevated sea surface temperatures have direct effects on coral microbiomes by promoting growth and virulence of opportunists and putative pathogens, thereby altering host immunity and health. However, interactions between these biotic and abiotic factors have yet to be evaluated. Here, we used a factorial experiment to investigate the combined effects of fecal pellet deposition by the widely distributed surgeonfish Ctenochaetus striatus and elevated sea surface temperatures on microbiomes associated with the reef-building coral Porites lobata. Our results showed that regardless of temperature, exposure of P. lobata to C. striatus feces increased alpha diversity, dispersion, and lead to a shift in microbial community composition – all indicative of microbial dysbiosis. Although elevated temperature did not result in significant changes in alpha and beta diversity, we noted an increasing number of differentially abundant taxa in corals exposed to both feces and thermal stress within the first 48h of the experiment. These included opportunistic microbial lineages and taxa closely related to potential coral pathogens (i.e., Vibrio vulnificus, Photobacterium rosenbergii). Some of these taxa were absent in controls but present in surgeonfish feces under both temperature regimes, suggesting mechanisms of microbial transmission and/or enrichment from fish feces to corals. Importantly, the impact to coral microbiomes by fish feces under higher temperatures appeared to inhibit wound healing in corals, as percentages of tissue recovery at the site of feces deposition were lower at 30°C compared to 26°C. Lower percentages of tissue recovery were associated with greater relative abundance of several bacterial lineages, with some of them found in surgeonfish feces (i.e., Rhodobacteraceae, Bdellovibrionaceae, Crocinitomicaceae). Our findings suggest that fish feces interact with elevated sea surface temperatures to favor microbial opportunism and enhance dysbiosis susceptibility in P. lobata. As the frequency and duration of thermal stress related events increase, the ability of coral microbiomes to recover from biotic stressors such as deposition of fish feces may be greatly affected, ultimately compromising coral health and resilience.

Consumer feces impact coral health in guild-specific ways

“…Herbivore activity thereby increases coral reef resilience under anthropogenic pressures and reduces the chance of phase shifts from coral- to algae-dominated states ( 70 ). Our research, as well as two previous studies ( 11, 21 ), add an additional dimension to this relationship: herbivores can also disperse pathogens in their feces that cause lesions in coral tissues. More work is needed to test the extent to which different (herbivorous) fish species contribute to the dispersal of viable coral pathogens ( 5 ).…”

Phosphate enrichment induces increased dominance of the parasiteAquarickettsiain the coralAcropora cervicornis

“…To avoid host DNA contamination, amplified samples were run on a 1.5% low melting point agarose gel until ∼1 cm separation was achieved between the off-target 12S rRNA host band and target product 16S rRNA band. Second-step PCR was conducted according to the methods described in Ezzat et al ( 2021 ) and Messyasz et al ( 2021 ). Each visible 16S band was poked with a sterile 10 µl plastic pipette tip, which was swirled into a barcoding master mix solution containing 12.5 μl AccuStart II ToughMix (2X), 9.5 μl PCR-grade water, and 1 μl (10 mM) each of custom forward and reverse barcodes (dual indices with custom adapters).…”

Nutrient Enrichment Predominantly Affects Low Diversity Microbiomes in a Marine Trophic Symbiosis between Algal Farming Fish and Corals

“…In addition, Ruegeria was more abundant in fish and algal matrix microbiomes, and certain strains of this bacteria can inhibit growth of Vibrio species in corals or may be opportunistic pathogens [ 85 ]. It is unclear whether these ASVs are being transmitted from either or both the algal matrix and fish to the coral, but their higher abundance in fish and algal matrix microbiomes indicates these hosts as potential vectors of these coral pathogens [ 26 , 27 , 81 ].…”

“…First-step PCR was conducted according to the reaction and thermocycler protocol described in Maher et al 2020 [ 54 ]. Second-step PCR was conducted according to the methods described in Ezzat et al 2021 [ 26 ]. Briefly, each 16S band visualized on a 1.5% agarose gel was poked with a pipette tip and swirled into a second-step barcoding master mix solution which was then run on a thermocycler for barcoding.…”

“…We also previously showed that fishes have the capability to share and transfer microbiome members with corals. This includes the potential coral pathogens Vibrio vulnificus and Photobacterium rosenbergii which significantly changed in abundance in corals exposed to Surgeonfish feces and thermal stress [ 26 ]. Parrotfish predation on corals also resulted in increased bacterial alpha diversity and the detection of both beneficial and opportunistic bacteria was only found on corals post predation, indicating direct transmission of bacteria from fish mouth to coral mucus and tissue, or indirectly facilitating bacterial growth or invasion within the coral or from the surrounding environment [ 27 ].…”