Stable and sporadic symbiotic communities of coral and algal holobionts

Abstract

Coral and algal holobionts are assemblages of macroorganisms and microorganisms, including viruses, Bacteria, Archaea, protists and fungi. Despite a decade of research, it remains unclear whether these associations are spatial–temporally stable or species-specific. We hypothesized that conflicting interpretations of the data arise from high noise associated with sporadic microbial symbionts overwhelming signatures of stable holobiont members. To test this hypothesis, the bacterial communities associated with three coral species (Acropora rosaria, Acropora hyacinthus and Porites lutea) and two algal guilds (crustose coralline algae and turf algae) from 131 samples were analyzed using a novel statistical approach termed the Abundance-Ubiquity (AU) test. The AU test determines whether a given bacterial species would be present given additional sampling effort (that is, stable) versus those species that are sporadically associated with a sample. Using the AU test, we show that coral and algal holobionts have a high-diversity group of stable symbionts. Stable symbionts are not exclusive to one species of coral or algae. No single bacterial species was ubiquitously associated with one host, showing that there is not strict heredity of the microbiome. In addition to the stable symbionts, there was a low-diversity community of sporadic symbionts whose abundance varied widely across individual holobionts of the same species. Identification of these two symbiont communities supports the holobiont model and calls into question the hologenome theory of evolution.

Evidence for rapid, tide-related shifts in the microbiome of the coral Coelastrea aspera

“…This example illustrates the issues associated with the core microbiome concept. Other studies have argued that defining microbiomes as either 'stable' and/or 'sporadic' symbiotic communities would be more beneficial (Hester et al 2015;Glasl et al 2016). Regardless of the exact definition, with an increase in studies reporting changes in microbial communities, a meaningful consensus on definitions may emerge if consistencies can be found between systems.…”

“…The nearby coastline supports both oyster and fish farms, and two of the bacteria detected with a high frequency on Day 2 in *4-yr-old corals have been formerly associated with shellfish farms (Fulvivirga) and fish diseases (Piscirickettsiaceae) (Nedashkovskaya et al 2007;Rozas and Enríquez 2014). It has been proposed that the microbiome can be separated into microbes that can be classed as 'transient' and more sporadic versus those that are more stable or sometimes referred to as 'core' members (Ainsworth et al 2015;Hester et al 2015;Sweet and Bulling 2017). A large proportion of the bacterial phylotypes found in this study fall into the category of 'transient' members (i.e., only present in relatively few samples with little to no consistency among replicate colonies).…”

“…nMDS plots were also developed for data collected on each day of sampling to illustrate the relative changes in community patterns with time. Differences in microbial community variability for coral age-day combinations were assessed as described by Hester et al (2015). The variation within each microbial community was estimated by embedding the dissimilarity measures (Bray-Curtis distance matrix) within Euclidean space, resulting in the two-dimensional distances between individual samples approximating compositional dissimilarity.…”

“…However, recently it has been recognized that, in addition to the algal symbionts, corals also host a highly diverse and specific microbiome which includes bacteria, archaea, fungi, protists and viruses (Rohwer et al 2002). Much less is known about this coral microbiome, particularly with respect to the dynamics of microbial partners through coral development (Thompson et al 2014), aging (Williams et al 2015) and their responses to changing environments (Morrow et al 2012;Hester et al 2015;Glasl et al 2016;Röthig et al 2016).…”

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

“…With these context dependent numbers, it is thus difficult to say whether corals have a higher richness of microbial taxa than other marine species. For example, turf and CCA each exhibited overall higher numbers of OTUs (18,926 and 9,559) than the three coral species compared (Acropora hyacinthus, A. rosaria, and Porites lutea) (951, 2,331, 4,018) (Hester et al, 2016). Similarly, algal (i.e., Dictyota bartayresiana, Halimeda opuntia, turf algae, and CCA) microbiomes were generally more diverse overall [ranging from 6.22 to 7.82 (Shannon Index)] than those in corals (ranging from 2.84 to 4.51) (Barott et al, 2011).…”