Parasitic ‘Candidatus Aquarickettsia rohweri’ is a marker of disease susceptibility in Acropora cervicornis but is lost during thermal stress

Abstract

Holobiont phenotype results from a combination of host and symbiont genotypes as well as from prevailing environmental conditions that alter the relationships among symbiotic members. Corals exemplify this concept, where shifts in the algal symbiont community can lead to some corals becoming more or less thermally tolerant. Despite linkage between coral bleaching and disease, the roles of symbiotic bacteria in holobiont resistance and susceptibility to disease remains less well understood. This study thus characterizes the microbiome of disease-resistant and-susceptible Acropora cervicornis coral genotypes (hereafter referred to simply as 'genotypes') before and after high temperature-mediated bleaching. We found that the intracellular bacterial parasite 'Ca. Aquarickettsia rohweri' was strikingly abundant in disease-susceptible genotypes. Diseaseresistant genotypes, however, had notably more diverse and even communities, with correspondingly low abundances of 'Ca. Aquarickettsia'. Bleaching caused a dramatic reduction of 'Ca. Aquarickettsia' within disease-susceptible corals and led to an increase in bacterial community dispersion, as well as the proliferation of opportunists. Our data support the hypothesis that 'Ca. Aquarickettsia' species increase coral disease risk through two mechanisms: (i) the creation of host nutritional deficiencies leading to a compromised host-symbiont state and (ii) the opening of niche space for potential pathogens during thermal stress.

Deciphering Coral Disease Dynamics: Integrating Host, Microbiome, and the Changing Environment

“…For example, a recently discovered yet common bacterial parasite, Candidatus Aquarickettsia, is commonly found in corals but proliferates when exposed to elevated nutrients reducing coral growth and increasing tissue loss and mortality (Shaver et al, 2017;Klinges et al, 2019). What's more, this parasite has been found to be associated with disease susceptibility in some coral genotype backgrounds (Klinges et al, 2020). Pathogenesis also may initiate from either an extrinsic, invading pathogen or from an intrinsic member of the microbiome sometimes referred to as a "pathobiont" (Sweet and Bulling, 2017) or "opportunistic."…”

“…This invasion by opportunists during an epizootic is likely a common feature of coral diseases. This is evident by the observation that several common Caribbean coral diseases, including yellow-band disease, dark-spot syndrome, white pox disease, and white plague, all of which do not display typical transmission dynamics characteristic of contagious diseases van Woesik, 2012, 2014;Klinges et al, 2020), suggesting intrinsic properties of the holobiont may play a large role in disease initiation and progression. In these cases, it is important to examine host organismal traits that affect disease susceptibility and environmental thresholds that serve as tipping points for disruption of microbiome homeostasis and disease induction rather than focusing on transmission dynamics of pathogens.…”

The Organelle in the Ointment: cryptic mitochondria account for many unknown sequences in cross-species microbiome comparisons

“…Corals are animals that exist in intimate symbiosis with a wide variety of microscopic symbionts including microbial eukaryotes, bacteria, archaea, viruses, and phages (1–3). Collectively, these coral associates and the cnidarian host animal are known as the coral holobiont.…”

“…The interactions of coral-associated microbes with their host and one another are complex, but of great interest due to their potential to modulate coral disease susceptibility (e.g. (1)) and responses to environmental stressors. Marker gene studies using small-subunit ribosomal RNA gene amplicons (SSU rRNA) have played a key role in describing the coral holobiont.…”

“…Recent studies have identified bacteria in the genus Aquarickettsia as of particular interest as mediators of coral health (1,17). However, as Aquarickettsia and other members of Midichloreaceae are - in relative terms - somewhat closely related to mitochondria, we wanted to test whether our expanded taxonomies might increase mis-annotation of these important coral symbionts as mitochondria.…”