White Syndrome-Affected Corals Have a Distinct Microbiome at Disease Lesion Fronts

Abstract

Coral tissue loss diseases, collectively known as white syndromes (WSs), induce significant mortality on reefs throughout the Indo-Pacific, yet definitive confirmation of WS etiologies remains elusive. In this study, we integrated ecological disease monitoring, bacterial community profiling, in situ visualization of microbehost interactions, and cellular responses of the host coral through an 18-month repeated-sampling regime. We assert that the observed pathogenesis of WS lesions on acroporid corals at Lizard Island (Great Barrier Reef) is not the result of apoptosis or infection by Vibrio bacteria, ciliates, fungi, cyanobacteria, or helminths. Histological analyses detected helminths, ciliates, fungi, and cyanobacteria in fewer than 25% of WS samples, and helminths and fungi were also observed in 12% of visually healthy samples. The abundances of Vibrio-affiliated sequences (assessed using 16S rRNA amplicon sequencing) did not differ significantly between health states and never exceeded 3.3% of reads in any individual sample. In situ visualization detected Vibrio bacteria only in summer WS lesion samples and revealed no signs of these bacteria in winter disease samples (or any healthy tissue samples), despite continued disease progression year round. However, a 4-fold increase in Rhodobacteraceaeaffiliated bacterial sequences at WS lesion fronts suggests that this group of bacteria could play a role in WS pathogenesis and/or serve as a diagnostic criterion for disease differentiation. While the causative agent(s) underlying WSs remains elusive, the microbial and cellular processes identified in this study will help to identify and differentiate visually similar but potentially distinct WS etiologies.IMPORTANCE Over the past decade, a virulent group of coral diseases known as white syndromes have impacted coral reefs throughout the Indian and Pacific Oceans. This article provides a detailed case study of white syndromes to combine disease ecology, high-throughput microbial community profiling, and cellular-scale host-microbe visualization over seasonal time scales. We provide novel insights into the etiology of this devastating disease and reveal new diagnostic criteria that could be used to differentiate visually similar but etiologically distinct forms of white syndrome.

Rhodobacterales and Rhizobiales Are Associated With Stony Coral Tissue Loss Disease and Its Suspected Sources of Transmission

“…A similar pattern is seen in freshwater microcystic blooms, on the first day Rhizobiales are one of the most abundant bacteria orders and after 2-4 days Rhizobiales decrease and Rhodobacterales become one of the most abundant orders (Li et al, 2011). Rhodobacterales are associated with multiple coral diseases, and this may not be because they are causative agents of disease, but rather they may be efficient successors and readily colonize diseased corals (Pollock et al, 2017). For example, corals inoculated with the known coral pathogen Vibrio coralliilyticus showed that initial timepoints had high relative abundances of Vibrionales, but hours later the relative abundances of Vibrionales decreased and relative abundances of Rhodobacterales increased (Welsh et al, 2017).…”

“…AH SINT from the vulnerable zone had different bacteria enriched compared with the endemic and epidemic zones (Figure 4D). Unlike in the vulnerable zone, AH SINT in the endemic and epidemic zones had three bacterial taxa that have been linked to coral diseases -including SCTLD: Cryomorphaceae (Gignoux-Wolfsohn et al, 2017;Meyer et al, 2019), Rhizobiaceae (Cárdenas et al, 2012;Meyer et al, 2019), and Rhodobacteraceae (Sunagawa et al, 2009;Cárdenas et al, 2012;Roder et al, 2014;Gignoux-Wolfsohn et al, 2017;Pollock et al, 2017;Meyer et al, 2019) (Figure 4D). Although AH colonies of the other two coral species also grouped by zones, colonies sampled in the epidemic and endemic zones did not show any signatures that would suggest that they were exposed to disease (Figures 4E,F).…”

“…However, Rhodobacterales are known to work together in the ocean to form biofilms (Elifantz et al, 2013), and this intrinsic cooperative behavior may aid in disease development or colonization on already diseased tissue (Parsek and Singh, 2003;Pollock et al, 2017). The EpDL network analysis showed multiple Rhodobacterales interacting with one another and acting as "key players" of the network (Figure 9).…”

Disentangling causation: complex roles of coral‐associated microorganisms in disease

“…This term has been introduced as a growing number of studies (not limited to coral), demonstrate shifts in the consortia of microbial communities linked with gross signs of compromised host health, rather than pointing at a single causative agent (reviewed in Vayssier‐Taussat et al ., ). Certain bacterial groups become more dominant in the pathobiome due to the complex interactions between environmental stress and the coral host (Pollock et al ., ; Vega Thurber et al ., ). In addition, it has been suggested recently that there is a ubiquitous core microbiome associated with corals that are likely beneficial to host health, together with the functional niche fillers and other highly variable microbial community members (Ainsworth et al ., ; Hernandez‐Agreda et al ., ; Peixoto et al ., ).…”

“…However, these traditional approaches have been argued to be challenging especially when applied to corals (for review see Richardson, 1998) and not suitable for polymicrobial diseases or microbial agents that cannot be cultured (Sato et al, 2016). Culture-independent molecular profiling of microbial communities targeting 16S rRNA gene sequences have also been extensively applied to disease lesions, to identify the microbial community composition associated with the diseased corals and directly compare them to healthy tissues (e.g., Cr oquer et al, 2013;Frias-lopez et al, 2004;Kimes et al, 2010;Meyer et al, 2014;Pantos and Bythell, 2006;Pollock et al, 2017;Soffer et al, 2015;Sunagawa et al, 2009). In some cases, causation has been inferred based on retrieval of sequences affiliated with previously characterized pathogens.…”