Intraspecific differences in molecular stress responses and coral pathobiome contribute to mortality under bacterial challenge in Acropora millepora

Abstract

Disease causes significant coral mortality worldwide; however, factors responsible for intraspecific variation in disease resistance remain unclear. We exposed fragments of eight Acropora millepora colonies (genotypes) to putatively pathogenic bacteria (Vibrio spp.). Genotypes varied from zero to >90% mortality, with bacterial challenge increasing average mortality rates 4–6 fold and shifting the microbiome in favor of stress-associated taxa. Constitutive immunity and subsequent immune and transcriptomic responses to the challenge were more prominent in high-mortality individuals, whereas low-mortality corals remained largely unaffected and maintained expression signatures of a healthier condition (i.e., did not launch a large stress response). Our results suggest that lesions appeared due to changes in the coral pathobiome (multiple bacterial species associated with disease) and general health deterioration after the biotic disturbance, rather than the direct activity of any specific pathogen. If diseases in nature arise because of weaknesses in holobiont physiology, instead of the virulence of any single etiological agent, environmental stressors compromising coral condition might play a larger role in disease outbreaks than is currently thought. To facilitate the diagnosis of compromised individuals, we developed and independently cross-validated a biomarker assay to predict mortality based on genes whose expression in asymptomatic individuals coincides with mortality rates.

Antimicrobial and stress responses to increased temperature and bacterial pathogen challenge in the holobiont of a reef‐building coral

“…Homologues of histamine receptors, which are known to regulate immuno‐stimulatory cytokine production (O'Mahony, Akdis, & Akdis, ) as well as a member of the solute carrier family 16 (SLC16A10), were upregulated. Increased expression of histamine receptors was recently also found in coral tissues affected by white syndrome, the disease caused by V. coralliilyticus (Wright et al., ), indicating that this might be a specific response to this pathogen. As SLC16A10 transports the PO substrate L‐DOPA (Kim et al., ), this suggests involvement of the melanization cascade in the anti‐ V. coralliilyticus response.…”

“…Cryptochrome, a repressor of expression of the CLOCK gene, was downregulated in response to bacterial challenges, which was likely linked to the upregulation of CLOCK . Reduced levels of cryptochrome have previously been linked to increased expression of pro‐inflammatory cytokines and inducible nitric oxide synthase, which plays a role in the antimicrobial oxidative burst following phagocytosis or encapsulation (Curtis et al., ) and was recently reported in pathogen‐challenged corals (Wright et al., ). In addition, CLOCK represses the anti‐inflammatory function of the glucocorticoid receptor, enhances the activity of NF‐κB and positively regulates the expression of Toll‐like receptors (e.g., TLR9) and their downstream transcription factors (FOS and JUN) (Curtis et al., ) (Scheiermann, Kunisaki, & Frenette, ).…”

Host genetics and geography influence microbiome composition in the spongeIrcinia campana

“…In other species, polymorphism in immunity-related genes has been found to affect microbiome composition (Bolnick et al, 2014;Kubinak et al, 2015;Pearce et al, 2017) and responses to pathogenic bacteria (Lazzaro, Sceurman, & Clark, 2004). In addition, genotype-specific immune response, and varying gene expression patterns in response to a potentially pathogenic bacteria, have been observed in the coral Acropora millepora (Wright et al, 2017). Although they do not have an acquired immune system, sponges have a relatively sophisticated innate immune system (Müller & Müller, 2003), which has been speculated to aid the maintenance of distinct extracellular microbial communities in the mesohyl tissue where phagocytosis of food bacteria takes place (Wehrl, Steinert, & Hentschel, 2007;Wilkinson, Garrone, & Vacelet, 1984).…”

Specific plasmid patterns and high rates of bacterial co‐occurrence within the coral holobiont

“…Corals can harbor complex microbial ecosystems, which frequently result in the development of both specific and variable host‐associated microbial communities (reviewed in Webster & Reusch, ), which can benefit host fitness (Peixoto, Rosado, Leite, Rosado, & Bourne, ; Webster & Reusch, ). Despite the close relationship between corals and their associated microbiomes, which can include organisms that have effects that vary from beneficial (Damjanovic, Blackall, Webster, & van Oppen, ; Krediet, Ritchie, Paul, & Teplitski, ; Peixoto et al., ; Webster & Reusch, ) to pathogenic (Meistertzheim, Nugues, Quéré, & Galand, ; Sweet & Bulling, ; Wright et al., ), knowledge of these intrinsic symbiotic, or dysbiotic, that is, disrupted symbiotic relationships (Bosch & Miller, ; Egan & Gardiner, ; Petersen & Round, ), interactions, and associated mechanisms is sparse.…”