Changes in coral-associated microbial communities during a bleaching event

Abstract

Environmental stressors such as increased sea surface temperatures are well-known for contributing to coral bleaching; however, the effect of increased temperatures and subsequent bleaching on coral-associated microbial communities is poorly understood. Colonies of the hard coral Acropora millepora were tagged on a reef flat off Magnetic Island (Great Barrier Reef) and surveyed over 2.5 years, which included a severe bleaching event in January/February 2002. Daily average water temperatures exceeded the previous 10-year average by more than 1 1C for extended periods with field-based visual surveys recording all tagged colonies displaying signs of bleaching. During the bleaching period, direct counts of coral zooxanthellae densities decreased by B64%, before recovery to pre-bleaching levels after the thermal stress event. A subset of three tagged coral colonies were sampled through the bleaching event and changes in the microbial community elucidated. Denaturing gradient gel electrophoresis (DGGE) analysis demonstrated conserved bacterial banding profiles between the three coral colonies, confirming previous studies highlighting specific microbial associations. As coral colonies bleached, the microbial community shifted and redundancy analysis (RDA) of DGGE banding patterns revealed a correlation of increasing temperature with the appearance of Vibrio-affiliated sequences. Interestingly, this shift to a Vibrio-dominated community commenced prior to visual signs of bleaching. Clone libraries hybridized with Vibrio-specific oligonucleotide probes confirmed an increase in the fraction of Vibrio-affiliated clones during the bleaching period. Post bleaching, the coral microbial associations again shifted, returning to a profile similar to the fingerprints prior to bleaching. This provided further evidence for corals selecting and shaping their microbial partners. For non-bleached samples, a close association with Spongiobacter-related sequences were revealed by both clone libraries and DGGE profiling. Despite Vibrio species being previously implicated in bleaching of specific coral species, it is unsure if the relative increase in retrieved Vibrio sequences is due to bacterial infection or an opportunistic response to compromised health and changing environmental parameters of the coral host. This study provides the first molecular-based study demonstrating changes in coral-associated bacterial assemblages during a bleaching event on a natural reef system.

The impact of reduced pH on the microbial community of the coral Acropora eurystoma

“…Another interesting finding we observed when examining the community in the corals exposed to pH 7.3 was the increase in species showing close homology to families that include known coral pathogens, such as Vibrionaceae and Alteromonadaceae (Ritchie, 2006;Bourne et al, 2007;Arboleda and Reichardt, 2009;Sunagawa et al, 2009), as well as Rhodobacteraceae (Alphaproteobacteria), previously isolated from diseased, injured or stressed marine invertebrates (Sekar et al, 2006;Sunagawa et al, 2009).…”

“…(GU726843) (see Supplementary Table S2). This change is especially interesting as species that belong to Vibrionaceae and Alteromonadaceae were previously associated with diseased or stressed corals (Ritchie, 2006;Bourne et al, 2007;Arboleda and Reichardt, 2009;Sunagawa et al, 2009).…”

Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome

“…Endozoicomonas are Gammaproteobacteria frequently observed in reef‐building corals (Bayer et al., 2013; Bourne et al., 2008; Glasl, Herndl, & Frade, 2016; Neave, Michell, et al., 2017; Neave, Rachmawati, et al., 2017; Pantos, Bongaerts, Dennis, Tyson, & Hoegh‐Guldberg, 2015; Pogoreutz, Rädecker, Cárdenas, Gärdes, Wild, et al., 2017) and highly dominant in pocilloporid hosts where they were found to reside deep within the gastrovascular tissues (Bayer et al., 2013; Neave, Rachmawati, et al., 2017). More generally, Endozoicomonas are commonly assumed to provide an important role in coral holobiont functioning due to their widespread prevalence and high abundance in many coral species (Bayer et al., 2013; Gignoux‐Wolfsohn, Aronson, & Vollmer, 2017; Glasl et al., 2016; Jessen et al., 2013; Meyer, Gunasekera, Scott, Paul, & Teplitski, 2016; Neave et al., 2016; Neave, Rachmawati, et al., 2017) and apparent metabolic versatility (Ding, Shiu, Chen, Chiang, & Tang, 2016; Hyun et al., 2014; Neave, Michell, et al., 2017; Yang et al., 2010).…”

Coral reef invertebrate microbiomes correlate with the presence of photosymbionts

“…The documented decline in coral reef ecosystems worldwide (Wilkinson, 2008) has prompted research into understanding how changing environmental conditions affect the close symbiotic associations of marine invertebrates (Webster et al, 2001;Bourne et al, 2008;Vega Thurber et al, 2008;Webster et al, 2008;Littman et al, 2010Littman et al, , 2011Webster et al, 2011). Only by studying marine invertebrates as holobionts (the host and all associated microbial communities) and better characterising the forces that structure their microbial associations will we be able to fully assess their capacity to adapt or acclimatise to environmental stress.…”