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

Naohisa Wada,Gal Eyal,Tetsuya Hayashi,Nalinee Thongtham,Omri Bronstein,Dai Yoshimura,Hideaki Yuasa,Zac Forsman,Nina Yasuda,Sen-Lin Tang,Rei Kajitani,Takehiko Itoh,Hugh Sweatman,Yoshitoshi Ogura,Atsushi Toyoda,Yukihiro Higashimura,Yasuhiro Gotoh

doi:10.1186/s40168-020-00880-3

Abstract

BackgroundPopulation outbreaks of the crown-of-thorns starfish (Acanthaster planci sensu lato; COTS), a primary predator of reef-building corals in the Indo-Pacific Ocean, are a major threat to coral reefs. While biological and ecological knowledge of COTS has been accumulating since the 1960s, little is known about its associated bacteria. The aim of this study was to provide fundamental information on the dominant COTS-associated bacteria through a multifaceted molecular approach.MethodsA total of 205 COTS individuals from 17 locations throughout the Indo-Pacific Ocean were examined for the presence of COTS-associated bacteria. We conducted 16S rRNA metabarcoding of COTS to determine the bacterial profiles of different parts of the body and generated a full-length 16S rRNA gene sequence from a single dominant bacterium, which we designated COTS27. We performed phylogenetic analysis to determine the taxonomy, screening of COTS27 across the Indo-Pacific, FISH to visualize it within the COTS tissues, and reconstruction of the bacterial genome from the hologenome sequence data.ResultsWe discovered that a single bacterium exists at high densities in the subcuticular space in COTS forming a biofilm-like structure between the cuticle and the epidermis. COTS27 belongs to a clade that presumably represents a distinct order (so-called marine spirochetes) in the phylum Spirochaetes and is universally present in COTS throughout the Indo-Pacific Ocean. The reconstructed genome of COTS27 includes some genetic traits that are probably linked to adaptation to marine environments and evolution as an extracellular endosymbiont in subcuticular spaces.ConclusionsCOTS27 can be found in three allopatric COTS species, ranging from the northern Red Sea to the Pacific, implying that the symbiotic relationship arose before the speciation events (approximately 2 million years ago). The universal association of COTS27 with COTS and nearly mono-specific association at least with the Indo-Pacific COTS provides a useful model system for studying symbiont-host interactions in marine invertebrates and may have applications for coral reef conservation.14hKu4n_u3gGCFxJyez66bVideo

Highlights

IntroductionPopulation outbreaks of a coral predator, the crown-of-thorns starfish (Acanthaster planci sensu lato; Crown-of-thorns starfish (COTS)), are a great threat to Indo-Pacific coral reef ecosystem integrity and biodiversity [3,4,5]
Coral reefs support almost one third of the world’s marine coastal species [1, 2]
Identification of a single Operational taxonomic unit (OTU) (COTS27) that dominates the body surface microbiota of Crown-of-thorns starfish (COTS) using 16S rRNA metabarcoding analysis We used 16S rRNA metabarcoding to analyse the bacterial composition of the microbiota in the body parts (7–8 body parts; disc spines [top and base], arm spines [top and base], ambulacral spines [top and base for Okinawa, or the whole spine for Miyazaki], tube feet, and pyloric stomachs; Fig. 1b) of six COTS individuals that were collected in Miyazaki and Okinawa, Japan

Summary

Introduction

Population outbreaks of a coral predator, the crown-of-thorns starfish (Acanthaster planci sensu lato; COTS), are a great threat to Indo-Pacific coral reef ecosystem integrity and biodiversity [3,4,5]. The bacterial symbionts of marine invertebrates have been shown to be important to their host organisms [7]. Extracellular endosymbionts known as subcuticular bacteria (SCB [16]) have been shown to reside under the cuticular layer of echinoderm fauna from all five extant classes, and it has been postulated that these bacteria provide dissolved free amino acids to their echinoderm hosts [9, 17]. Population outbreaks of the crown-of-thorns starfish (Acanthaster planci sensu lato; COTS), a primary predator of reef-building corals in the Indo-Pacific Ocean, are a major threat to coral reefs. The aim of this study was to provide fundamental information on the dominant COTS-associated bacteria through a multifaceted molecular approach

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