Allelochemicals produced by Caribbean macroalgae and cyanobacteria have species-specific effects on reef coral microorganisms

Abstract

Coral populations have precipitously declined on Caribbean reefs while algal abundance has increased, leading to enhanced competitive damage to corals, which likely is mediated by the potent allelochemicals produced by both macroalgae and benthic cyanobacteria. Allelochemicals may affect the composition and abundance of coral-associated microorganisms that control host responses and adaptations to environmental change, including susceptibility to bacterial diseases. Here, we demonstrate that extracts of six Caribbean macroalgae and two benthic cyanobacteria have both inhibitory and stimulatory effects on bacterial taxa cultured from the surfaces of Caribbean corals, macroalgae, and corals exposed to macroalgal extracts. The growth of 54 bacterial isolates was monitored in the presence of lipophilic and hydrophilic crude extracts derived from Caribbean macroalgae and cyanobacteria using 96-well plate bioassays. All 54 bacterial cultures were identified by ribotyping. Lipophilic extracts from two species of Dictyota brown algae inhibited[50% of the reef coral bacteria assayed, and hydrophilic compounds from Dictyota menstrualis particularly inhibited Vibrio bacteria, a genus associated with several coral diseases. In contrast, both lipo-and hydrophilic extracts from 2 species of Lyngbya cyanobacteria strongly stimulated bacterial growth. The brown alga Lobophora variegata produced hydrophilic compounds with broad-spectrum antibacterial effects, which inhibited 93% of the bacterial cultures. Furthermore, bacteria cultured from different locations (corals vs. macroalgae vs. coral surfaces exposed to macroalgal extracts) responded differently to algal extracts. These results reveal that extracts from macroalgae and cyanobacteria have species-specific effects on the composition of coral-microbial assemblages, which in turn may increase coral host susceptibility to disease and result in coral mortality.

Microbial to reef scale interactions between the reef-building coral Montastraea annularis and benthic algae

“…Further investigations are needed to determine the direct effects of these interface-associated microbial communities on coral health. Recent studies have shown that different species of algae alter the growth of coral bacteria [61], supporting the hypothesis that algae may directly alter the structure of the coral holobiont.…”

Allelochemicals Produced by Brown Macroalgae of the Lobophora Genus Are Active against Coral Larvae and Associated Bacteria, Supporting Pathogenic Shifts to Vibrio Dominance

“…Direct contact with Lobophora macroalgae has already been shown to cause a negative physiological effect on corals in the form of tissue necrosis and bleaching (7,9,14,15,47,48). Previous studies have also shown that crude extracts from Caribbean L. variegata, particularly hydrophilic compounds, have broadspectrum antibacterial activity that causes significant shifts in coral-associated microbial communities (13,21). Thus, while most other studies have focused on lipophilic organic compounds from macroalgae, the current study builds on previous microbial community profiling data (21) and further indicates that aqueous compounds produced by Lobophora sp.…”

“…They also found that Porites cylindrica was the most resistant to macroalgal damage based on visual assessments (9). Direct contact between macroalgae and corals has been implicated in reduced coral growth and fecundity, bleaching, tissue necrosis, mortality, and disease (7)(8)(9)(10)(11)(12)(13)(14)(15). Macroalgae have also been shown to indirectly induce and inhibit coral larval settlement (16,17), both of which are likely to result in larval mortality via poor substratum choice (e.g., shading, overgrowth, and ephemeral growth), mechanical damage (e.g., algal abrasion), or allelochemical defenses.…”

“…Each coral species maintains a specific assemblage of microorganisms that may be influenced by interactions with macroalgae (13,20,21). Numerous studies have shown that shifts in microbial community composition can be detrimental to coral health and may predispose corals to bleaching, infection, and mortality (26,27).…”

“…Lipophilic compounds from Lobophora variegata have been shown to be chemically damaging to most corals (14), and they produce allelopathic activity against pathogenic and saprophytic marine fungi (36). Hydrophilic (i.e., water-soluble) compounds produced by L. variegata demonstrated antibacterial activity against 93% of coral reef bacterial isolates, while lipophilic compounds caused significant growth in 94% of the isolates tested (13). Both aqueous and organic crude extracts from L. variegata were also shown to cause significant shifts in the microbial communities associated with two common Caribbean corals, Orbicella faveolata and Porites astreoides (21).…”