The Microbial Signature Provides Insight into the Mechanistic Basis of Coral Success across Reef Habitats

Abstract

For ecosystems vulnerable to environmental change, understanding the spatiotemporal stability of functionally crucial symbioses is fundamental to determining the mechanisms by which these ecosystems may persist. The coral Pachyseris speciosa is a successful environmental generalist that succeeds in diverse reef habitats. The generalist nature of this coral suggests it may have the capacity to form functionally significant microbial partnerships to facilitate access to a range of nutritional sources within different habitats. Here, we propose that coral is a metaorganism hosting three functionally distinct microbial interactions: a ubiquitous core microbiome of very few symbiotic host-selected bacteria, a microbiome of spatially and/or regionally explicit core microbes filling functional niches (<100 phylotypes), and a highly variable bacterial community that is responsive to biotic and abiotic processes across spatial and temporal scales (>100,000 phylotypes). We find that this coral hosts upwards of 170,000 distinct phylotypes and provide evidence for the persistence of a select group of bacteria in corals across environmental habitats of the Great Barrier Reef and Coral Sea. We further show that a higher number of bacteria are consistently associated with corals on mesophotic reefs than on shallow reefs. An increase in microbial diversity with depth suggests reliance by this coral on bacteria for nutrient acquisition on reefs exposed to nutrient upwelling. Understanding the complex microbial communities of host organisms across broad biotic and abiotic environments as functionally distinct microbiomes can provide insight into those interactions that are ubiquitous niche symbioses and those that provide competitive advantage within the hosts’ environment.

Distinct Bacterial Microbiomes Associate with the Deep-Sea Coral Eguchipsammia fistula from the Red Sea and from Aquaria Settings

“…In particular, adjustment of associated bacteria to prevailing environmental conditions has been suggested to support acclimatization of the coral holobiont (Reshef et al, 2006). This notion is supported by recent studies that show, at least in part, flexible bacterial microbiomes of the coral holobiont to environmental change (Jessen et al, 2013;Roder et al, 2015;Hernandez-Agreda et al, 2016;Röthig et al, 2016;Ziegler et al, 2016Ziegler et al, , 2017. However, our knowledge on the role of the bacterial microbiome to coral holobiont function is still limited (Bourne and Webster, 2013;Bourne et al, 2016), although bacteria are shown to contribute to coral health (Rosenberg et al, 2007;Krediet et al, 2013) and are involved in nutrient cycling (Rädecker et al, 2015;Bourne et al, 2016).…”

“…More importantly, these microbiomes align functionally to the different environments (see below). As such, the notion of species-specific core microbiomes that are consistent over large geographical and environmental scales (Bayer et al, 2013a;Ainsworth et al, 2015;Roder et al, 2015;Hernandez-Agreda et al, 2016Ziegler et al, 2016;Neave et al, 2017) is in contrast to the highly variable core microbiome in E. fistula. Rather, it may suggest a limited association with obligate bacterial symbionts and/or a high flexibility in regard to bacterial symbionts.…”

“…Coral microbiomes are shown to vary to a degree across spatial, depth, and environmental distributions (Pantos et al, 2015;Roder et al, 2015;Hernandez-Agreda et al, 2016;Glasl et al, 2017). Rapid adjustment of the microbiome has also recently been reported under stressful environmental conditions and suggested to support holobiont functioning (Röthig et al, 2016;Ziegler et al, 2017).…”

“…OTU0003 (P. angustum, previously Vibrio angustum/fischeri) was previously described as a squid endosymbiont and closely related taxa are shown to inhibit virulence gene expression (Thompson et al, 2009;Mansson et al, 2011), at least hypothetically indicating functional importance and a potential to form a symbiotic relationship with a metazoan host as suggested by Hernandez-Agreda et al (2016). OTU0086 (P. puraquae) has been identified as a coral-derived endophytic bacterium (Deng et al, 2015).…”

Rapid adaptive responses to climate change in corals

“…For example, transplantation of corals to a warmer environment resulted in shifts in the associated bacterial community that correlated with increased holobiont thermotolerance 87 . Additionally, higher bacterial diversity in deep compared to shallow water corals 88,89 suggests that some deep habitat-specific microbes may be involved in nutrient cycling specific to the low-irradiance environments. Both genetic and epigenetic processes contribute to high phenotypic plasticity and rapid evolution in bacteria 90 .…”