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

Abstract

Pervasive environmental stressors on coral reefs are attributed with shifting the competitive balance in favor of alternative dominants, such as macroalgae. Previous studies have demonstrated that macroalgae compete with corals via a number of mechanisms, including the production of potent primary and secondary metabolites that can influence coral-associated microbial communities. The present study investigates the effects of the Pacific brown macroalga Lobophora sp. (due to the shifting nature of the Lobophora species complex, it will be referred to here as Lobophora sp.) on coral bacterial isolates, coral larvae, and the microbiome associated with the coral Porites cylindrica. Crude aqueous and organic macroalgal extracts were found to inhibit the growth of coral-associated bacteria. Extracts and fractions were also shown to inhibit coral larval settlement and cause mortality at concentrations lower (Ͻ0.3 mg · ml Ϫ1 ) than calculated natural concentrations (4.4 mg · ml Ϫ1 ). Microbial communities associated with coral tissues exposed to aqueous (e.g., hydrophilic) crude extracts demonstrated a significant shift to Vibrio dominance and a loss of sequences related to the putative coral bacterial symbiont, Endozoicomonas sp., based on 16S rRNA amplicon sequencing. This study contributes to growing evidence that macroalgal allelochemicals, dissolved organic material, and native macroalgal microbial assemblages all play a role in shifting the microbial equilibrium of the coral holobiont away from a beneficial state, contributing to a decline in coral fitness and a shift in ecosystem structure.IMPORTANCE Diverse microbial communities associate with coral tissues and mucus, providing important protective and nutritional services, but once disturbed, the microbial equilibrium may shift from a beneficial state to one that is detrimental or pathogenic. Macroalgae (e.g., seaweeds) can physically and chemically interact with corals, causing abrasion, bleaching, and overall stress. This study contributes to a growing body of evidence suggesting that macroalgae play a critical role in shifting the coral holobiont equilibrium, which may promote the invasion of opportunistic pathogens and cause coral mortality, facilitating additional macroalgal growth and invasion in the reef. Thus, macroalgae not only contribute to a decline in coral fitness but also influence coral reef ecosystem structure.KEYWORDS DNA sequencing, Lobophora, Porites, QIIME, coral larvae, coral reef, holobiont, macroalgae, metagenomics, pathogens

Intergenerational effects of macroalgae on a reef coral: major declines in larval survival but subtle changes in microbiomes

“…This result contrasts with evidence suggesting that macroalgae alter the physiochemical environment, the microbial load, and community composition in surrounding seawater (Wild et al 2010, Haas et al 2011, Nelson et al 2013), and the microbiome of associated corals (Wild et al 2010, Haas et al 2011, Morrow et al 2012, 2013, 2017, Thurber et al 2012, Nelson et al 2013). Specifically, algae are predicted to affect corals through DOM release that promotes microbial growth in surrounding seawater, declines in local oxygen concentrations, and enrichment of copiotrophic and pathogenic microbes that may overwhelm the native coral microbiota (Dinsdale & Rohwer 2011, Barott & Rohwer 2012).…”

“…Specifically, algae are predicted to affect corals through DOM release that promotes microbial growth in surrounding seawater, declines in local oxygen concentrations, and enrichment of copiotrophic and pathogenic microbes that may overwhelm the native coral microbiota (Dinsdale & Rohwer 2011, Barott & Rohwer 2012). Algae may also release allelochemicals that alter coral microbial communities on contact (Morrow et al 2011, 2012, 2017), or act as vectors for pathogenic microbes (Nugues et al 2004, Sweet et al 2013). All of these mechanisms may operate on relatively small spatial scales, exerting strongest effects in zones of direct algae-coral contact (Barott et al 2009, 2011, Pratte et al 2017).…”

“…These stressors may directly harm corals, but may also indirectly lower coral health by allowing proliferation of competitive macroalgae (Hughes et al 2010). Contact with algae has been linked to bleaching, disease, and tissue death in adult corals (Nugues et al 2004, Rasher and Hay 2010), potentially harming coral through diverse mechanisms, including allelopathy, oxygen depletion, and destabilization of coral-associated microbial communities (microbiomes) (Rasher & Hay 2010, Barott & Rohwer 2012, Zaneveld et al 2016, Morrow et al 2017). Furthermore, macroalgae can directly inhibit both settlement and survivorship of coral larvae (Kuffner et al 2006, Hughes et al 2007, Dixson et al 2014, Webster et al 2015), often in a species-specific manner (Vermeij et al 2009).…”

“…Coral-macroalgae interactions on degraded reefs may drive dysbiosis, shifting the coral microbiome to an alternative state via mechanisms such as the production of algal allelochemicals (Morrow et al 2012, Morrow et al 2017), release of dissolved organic matter (Dinsdale & Rohwer 2011, Barott & Rohwer 2012, Haas et al 2016), or transfer of harmful bacteria to corals interacting with algae (Nugues et al 2004, Sweet et al 2013, Pratte et al 2017). Alternatively, changes in coral microbiomes in response to increasing algal cover could be a mechanism by which corals cope with algal competition or other biotic and abiotic stressors (Rosenberg et al 2007).…”

Responses of Coral-Associated Bacterial Communities to Local and Global Stressors

“…However, this is not always the case, as other studies have demonstrated no significant change or a decrease in microbial diversity under these three stressors (Meron et al, 2012;Tracy et al, 2015;Morrow et al, 2017). These conflicting results likely are the result of variability in coral microbiome responses across coral host species, locations and stressors.…”