Crown-of-Thorns Sea Star Acanthaster cf. solaris Has Tissue-Characteristic Microbiomes with Potential Roles in Health and Reproduction

Abstract

Outbreaks of coral-eating crown-of-thorns sea stars (CoTS; Acanthaster species complex) cause substantial coral loss; hence, there is considerable interest in developing prevention and control strategies. We characterized the microbiome of captive CoTS and assessed whether dysbiosis was evident in sea stars during a disease event. Most tissue types had a distinct microbiome. The exception was female gonads, in which the microbiomes were highly variable among individuals. Male gonads were dominated (>97% of reads) by a single Mollicutes-related operational taxonomic unit (OTU). Detailed phylogenetic and microscopy analysis demonstrated the presence of a novel Spiroplasma-related bacterium in the spermatogenic layer. Body wall samples had high relative abundance (43 to 64% of reads) of spirochetes, likely corresponding to subcuticular symbionts reported from many echinoderms. Tube feet were characterized by Hyphomonadaceae (24 to 55% of reads). Pyloric cecal microbiomes had high alpha diversity, comprising many taxa commonly found in gastrointestinal systems. The order Oceanospirillales (genera Endozoicomonas and Kistimonas) was detected in all tissues. A microbiome shift occurred in diseased individuals although differences between tissue types were retained. The relative abundance of spirochetes was significantly reduced in diseased individuals. Kistimonas was present in all diseased individuals and significantly associated with diseased tube feet, but its role in disease causation is unknown. While Arcobacter was significantly associated with diseased tissues and Vibrionaceae increased in diversity, no single OTU was detected in all diseased individuals, suggesting opportunistic proliferation of these taxa in this case. This study shows that CoTS have tissue-characteristic bacterial communities and identifies taxa that could play a role in reproduction and host health.IMPORTANCE Coral-eating crown-of-thorns sea stars (CoTS; Acanthaster species complex) are native to the Indo-Pacific, but during periodic population outbreaks they can reach extreme densities (>1,000 starfish per hectare) and function as a pest species. On the Great Barrier Reef, Australia, CoTS have long been considered one of the major contributors to coral loss. There has been significant investment in a targeted control program using lethal injection, and there is interest in developing additional and complementary technologies that can increase culling efficiencies. The biology of CoTS has been studied extensively, but little is known about their associated microbiome. This cultivation-independent analysis of the CoTS microbiome provides a baseline for future analyses targeting the functional role of symbionts, the identification of pathogens, or the development of reproduction manipulators.

The Microbial Landscape of Sea Stars and the Anatomical and Interspecies Variability of Their Microbiome

“…More recently, culture-independent approaches have been taken to characterize the microbial community associated with adult sea stars of Acanthaster cf. solaris (Crown-of-thorns star), Asterias amurensis (Japanese common star), and Patiria pectinifera (Blue bat star) ( Nakagawa et al, 2017 ; Høj et al, 2018 ). Direct comparisons between studies is difficult because of varying sampling approaches, PCR protocols, and bioinformatics analyses used though broad similarities of microbial community composition found between studies do arise.…”

“…The high relative abundance of Helicobacter -related taxon found previously in the coelomic fluid of Asterias amurensis was significantly less (<1% relative abundance) among the sea star taxa presented in this study ( Nakagawa et al, 2017 ). Previous work documenting microbial communities associated with Crown-of-thorns sea star found four major bacterial groups driving tissue-specific patterns which included Spirochaetales , Rhodobacterales , Oceanospirillales , and Mollicutes ( Høj et al, 2018 ). Our results corroborate these finding with the addition of Chromatiales and Enterobacteriales also making up observable differences between sample types ( Figures 6 , 7 ).…”

“…Recent functional predictions have been largely based on 16s rRNA community composition studies which are not a good predictor of community function. Nevertheless, current hypotheses regarding benefits provided by microbial symbionts include: sulfide detoxification, antifouling prevention, opportunistic pathogens, nitrogen fixation and nutrient acquisition ( Lawrence et al, 2010 ; Nakagawa et al, 2017 ; Høj et al, 2018 ). Nitrogenase activity has been found in the gastrointestinal tract of sea urchins.…”

A universal subcuticular bacterial symbiont of a coral predator, the crown-of-thorns starfish, in the Indo-Pacific

“…FQ660021.1). Hereafter, we refer to these spirochetes as "marine spirochetes", as referred to by Høj et al (2018) [21]. These marine spirochetes formed a distinct cluster within the phylum Spirochaetes, with the order Brachyspirales being their closest relative ( Fig.…”

“…Carrier et al reported shifts in COTS larval microbiomes with diet [20]. Høj et al found that adult COTS have tissue-specific bacterial communities, largely comprising four major bacterial groups: Mollicutes in male gonads, Spirochaetales in the body wall, Hyphomonadaxeae in the tube feet, and Oceanospirillales in all tissues [21]. Although these studies significantly increased our understanding of the COTS microbiome, there is still a great lack of knowledge regarding COTSassociated bacteria, particularly SCB.…”