Microbial mat compositions and localization patterns explain the virulence of black band disease in corals

Abstract

Black band disease (BBD) in corals is characterized by a distinctive, band-like microbial mat, which spreads across the tissues and often kills infected colonies. The microbial mat is dominated by cyanobacteria but also commonly contains sulfide-oxidizing bacteria (SOB), sulfate-reducing bacteria (SRB), and other microbes. The migration rate in BBD varies across different environmental conditions, including temperature, light, and pH. However, whether variations in the migration rates reflect differences in the microbial consortium within the BBD mat remains unknown. Here, we show that the micro-scale surface structure, bacterial composition, and spatial distribution differed across BBD lesions with different migration rates. The migration rate was positively correlated with the relative abundance of potential SOBs belonging to Arcobacteraceae localized in the middle layer within the mat and negatively correlated with the relative abundance of other potential SOBs belonging to Rhodobacteraceae. Our study highlights the microbial composition in BBD as an important determinant of virulence.

Divide and conquer: Spatial and temporal resource partitioning structures benthic cyanobacterial mats

“…This sustains anoxic and sulfidic conditions and provides a niche for the consortium of BBD‐causing bacteria (Carlton & Richardson, 1995). A BBD migration rate across a coral surface is directly affected by initial bacterial abundance, which can speed up the disease process (Wada et al., 2023). For bacterial members involved in BBD, resistance to sulfide is key, and this allows them to survive within the BBD band niche space (Meyer et al., 2017).…”

“…Mats form to create functionally similar communities across environments and are thus thought to form via deterministic processes (Stegen et al., 2012). Succession of early mat microbial members facilitates further colonization by other members by stabilizing areas of sediment through EPS, which is especially key in temperate marine habitats but present across ecosystems (Boomer et al., 2009; Gerbersdorf & Wieprecht, 2015; Wada et al., 2023). Succession is thus limited by recruitment and dispersal, filtering which members are able to colonize the existing mat (Tilman, 1994).…”

“…On coral reefs, mat proliferation directly smothers benthic invertebrates and can block coral settlement, inhibiting coral recruitment (Kuffner et al., 2006; Paul et al., 2005; Ribeiro et al., 2022; Ritson‐Williams et al., 2020). In addition, BCMs can act as reservoirs and potential vectors for pathogenic bacteria and are especially implicated in black band disease (BBD), a disease in which microbial members alter oxygen and sulfide dynamics of coral with destructive results (Carlton & Richardson, 1995; Cissell et al., 2022; Meyer et al., 2017; Myers et al., 2007; Sato et al., 2016, 2017; Wada et al., 2023). Additionally, removal of mat consumers due to anthropogenic pressures has increased BCM proliferation and community stability by removing natural top‐down controls (Cissell & McCoy, 2022; Ford et al., 2018).…”

The Impact of Tetrodotoxin (TTX) on the Gut Microbiome in Juvenile Tiger Pufferfish, Takifugu rubripes

“…TTX administration might enhance the proliferation of Arcobacter and other residential bacteria by inhibiting the growth of other bacteria. Previous research has suggested that the abundance of Arcobacter may be bene cial for the host rather than pathogenic host due to its metabolic capabilities for sulfur oxidation and carbon xation, as well as its ability to resist viruses in hag sh [17,47,122,68]. Previous study [112] reported that TTXfed sh exhibited the greatest growth at 8.5 ppt, followed by 34.0 ppt.…”

“…Additionally, it was found to be dominant in the ulcer mucus surfaces of Atlantic salmon, gut microbiota of hag sh, and giant abalone (Haliotis gigantea) [54,73,68,86]. Arcobacter species have a strong possibility of having the metabolic capacity for sulfur oxidation coupled with N-oxide reduction while xing carbon via the reverse TCA cycle [17,47,122]. Additionally, it is speculated that this species might possess the ability to resist viruses, potentially assisting in alleviating viral pressure [68].…”