Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages

Abstract

Increasing algal cover on tropical reefs worldwide may be maintained through feedbacks whereby algae outcompete coral by altering microbial activity. We hypothesized that algae and coral release compositionally distinct exudates that differentially alter bacterioplankton growth and community structure. We collected exudates from the dominant hermatypic coral holobiont Porites spp. and three dominant macroalgae (one each Ochrophyta, Rhodophyta and Chlorophyta) from reefs of Mo'orea, French Polynesia. We characterized exudates by measuring dissolved organic carbon (DOC) and fractional dissolved combined neutral sugars (DCNSs) and subsequently tracked bacterioplankton responses to each exudate over 48 h, assessing cellular growth, DOC/DCNS utilization and changes in taxonomic composition (via 16S rRNA amplicon pyrosequencing). Fleshy macroalgal exudates were enriched in the DCNS components fucose (Ochrophyta) and galactose (Rhodophyta); coral and calcareous algal exudates were enriched in total DCNS but in the same component proportions as ambient seawater. Rates of bacterioplankton growth and DOC utilization were significantly higher in algal exudate treatments than in coral exudate and control incubations with each community selectively removing different DCNS components. Coral exudates engendered the smallest shift in overall bacterioplankton community structure, maintained high diversity and enriched taxa from Alphaproteobacteria lineages containing cultured representatives with relatively few virulence factors (VFs) (Hyphomonadaceae and Erythrobacteraceae). In contrast, macroalgal exudates selected for less diverse communities heavily enriched in copiotrophic Gammaproteobacteria lineages containing cultured pathogens with increased VFs (Vibrionaceae and Pseudoalteromonadaceae). Our results demonstrate that algal exudates are enriched in DCNS components, foster rapid growth of bacterioplankton and select for bacterial populations with more potential VFs than coral exudates.

Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors

“…The current study confirms and extends earlier findings (27) by demonstrating similar correlations between benthic community composition and the enrichment of specific microbial taxa on coral reefs in situ (Table 1). Consistent with the effects of individual exudates, high coral cover was associated with higher abundances of Alphaproteobacteria, whereas the abundant fleshy macroalgae at Tabuaeran and Teraina were accompanied by more Gammaproteobacteria (e.g., Enterobacteriales and Pseudomonadales).…”

“…In addition, the microbial communities sampled on these reefs reflected selection by the adjacent benthic macroorganisms, as evidenced by the differences between reef-associated bacterioplankton communities and open ocean communities (26). There is evidence that reef-associated communities undergo selection in shallow reef environments by the locally available labile organic matter exuded by the benthic organisms (27). For example, in an empirical study, Nelson et al demonstrated that exudates collected from coral and macroalgae selectively fostered growth of distinct bacterioplankton communities (27).…”

“…There is evidence that reef-associated communities undergo selection in shallow reef environments by the locally available labile organic matter exuded by the benthic organisms (27). For example, in an empirical study, Nelson et al demonstrated that exudates collected from coral and macroalgae selectively fostered growth of distinct bacterioplankton communities (27). Coral exudates promoted communities with higher diversity, including lineages of Alphaproteobacteria with relatively few virulence factors (e.g., Erythrobacteraceae); whereas exudates from fleshy macroalgae selected for less diverse communities with more copiotrophic Gammaproteobacteria lineages (e.g., the families Alteromonadaceae, Pseudoalteromonadaceae, and Vibrionaceae).…”

“…S1). Increased coverage by fleshy algae selects for specific microbes that may be detrimental to coral health (27,35), thereby opening additional benthic space for further algal colonization (36).…”

Energetic differences between bacterioplankton trophic groups and coral reef resistance

“…DDAM predicts that stressors such as overfishing and eutrophication release turf and fleshy macroalgae from grazing control, leading to increased release rates of labile DOC. DOC stimulates heterotrophic microbial growth [18][19][20][21], some of which are opportunistic coral pathogens [22]. These pathogens kill corals and create more space for the algae.…”