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Appl Environ Microbiol
2018 Jun 18;8413:. doi: 10.1128/AEM.00181-18.
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Crown-of-Thorns Sea Star Acanthaster cf. solaris Has Tissue-Characteristic Microbiomes with Potential Roles in Health and Reproduction.
Høj L
,
Levy N
,
Baillie BK
,
Clode PL
,
Strohmaier RC
,
Siboni N
,
Webster NS
,
Uthicke S
,
Bourne DG
.
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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.
FIG 1. Schematic drawing of Acanthaster cf. solaris showing the location of sampled somatic tissues (body wall, tube feet, and pyloric ceca) and gonads.
FIG 2. Taxonomic composition of amplicon sequences from healthy Acanthaster cf. solaris tissue samples. Labels reflect the phylum (abbreviated), class, and order as assigned by the QIIME pipeline. OTUs that could not be assigned to a taxonomic group by the QIIME pipeline are categorized as unassigned, with the exception of two OTUs (Unassigned_OTU1 and Unassigned_OTU2) categorized as marine spirochetes based on their best BLAST matches, as discussed in the text. Orders with relative abundances of >1% in at least one sample are shown, with remaining taxa included in the category âother.â Abbreviations: A, Actinobacteria; B, Bacteroidetes; C, Cyanobacteria; F, Firmicutes: G, Gemmatimonadetes; P, Proteobacteria; T, Tenericutes; MG, male gonads; FG, female gonads; HBW, healthy body wall; HTF, healthy tube feet; HPC, healthy pyloric ceca. The associated number identifies the sampled individual as described in Table S5 in the supplemental material.
FIG 3. Principal-coordinate analysis (PCoA) plot based on Bray-Curtis similarities of Hellinger (square root)-transformed OTU abundance data evenly subsampled to 7,824 reads. Abbreviations: HBW, healthy body wall; HTF, healthy tube feet; HPC, healthy pyloric ceca; FG, female gonads; MG, male gonads. The number in the sample label identifies the sampled individual as described in Table S5 in the supplemental material.
FIG 4. Maximum likelihood tree showing the phylogenetic position within the Mollicutes of the dominant bacterium in Acanthaster cf. solaris male gonads. The sequence MG_clone14 was cloned from male gonads of Acanthaster cf. solaris collected from the Great Barrier Reef. The sequence MG_ oki_scaffold215 was extracted from an existing scaffold produced from male gonads of Acanthaster cf. solaris collected near Okinawa (5). Bootstrap values are based on 1,000 bootstrap replications. The scale bar represents the number of substitutions per site. GenBank accession numbers are given in parentheses.
FIG 5. Transmission electron micrographs from healthy Acanthaster cf. solaris tissues. (A) The spermatogenic layer of a male gonad showing bacterial morphologies (arrowheads) similar to those of Spiroplasma in exponential growth and its pleiomorphic or intermediate forms. Scale bar, 1 μm. (B) A spirochete-shaped bacterium (arrowhead) detected in the coelomic epithelium of tube feet. Scale bar, 500 nm.
FIG 6. Proportion of reads classified as Oceanospirillales and Endozoicomonaceae by QIIME for healthy and diseased Acanthaster cf. solaris tissue samples. Abbreviations: H, healthy; D, diseased; BW, body wall; TF, tube feet; PC, pyloric ceca. The number in the sample label identifies the sampled individual as described in Table S5 in the supplemental material.
FIG 7. Photos and micrographs showing representative healthy and diseased Acanthaster cf. solaris samples. The micrographs were produced by automated tiling and stitching as indicated. (a and b) Arms of healthy (a) and diseased (b) individuals. (c to h) The following hematoxylin- and eosin-stained tissue sections are also shown: body wall from healthy (c) and diseased (d) individuals (5-by-5 tiles, 10à objective; scale bar, 500 μm); tube feet from healthy (e) and diseased (f) individuals (5-by-5 tiles; 20à objective; scale bar, 200 μm); pyloric ceca from healthy (g) and diseased (h) individuals (4-by-4 tiles; 20à objective; scale bar, 200 μm).
Anbutsu,
Spiroplasma as a model insect endosymbiont.
2011, Pubmed
Anbutsu,
Spiroplasma as a model insect endosymbiont.
2011,
Pubmed
Austin,
The bacterial microflora of fish, revised.
2006,
Pubmed
Berry,
Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis.
2012,
Pubmed
Burnett,
Subcuticular bacteria from the brittle star Ophiactis balli (Echinodermata: Ophiuroidea) represent a new lineage of extracellular marine symbionts in the alpha subdivision of the class Proteobacteria.
1997,
Pubmed
,
Echinobase
Caporaso,
QIIME allows analysis of high-throughput community sequencing data.
2010,
Pubmed
Choi,
Kistimonas asteriae gen. nov., sp. nov., a gammaproteobacterium isolated from Asterias amurensis.
2010,
Pubmed
,
Echinobase
Clark,
Pathogenicity of mollicutes for insects: possible use in biological control.
1984,
Pubmed
Collado,
Taxonomy, epidemiology, and clinical relevance of the genus Arcobacter.
2011,
Pubmed
Cortés-Lara,
Prokaryotic microbiota in the digestive cavity of the jellyfish Cotylorhiza tuberculata.
2015,
Pubmed
De'ath,
The 27-year decline of coral cover on the Great Barrier Reef and its causes.
2012,
Pubmed
,
Echinobase
Duperron,
A tale of two chitons: is habitat specialisation linked to distinct associated bacterial communities?
2013,
Pubmed
Durand,
Microbial diversity associated with the hydrothermal shrimp Rimicaris exoculata gut and occurrence of a resident microbial community.
2010,
Pubmed
Edgar,
Search and clustering orders of magnitude faster than BLAST.
2010,
Pubmed
Egan,
Microbial Dysbiosis: Rethinking Disease in Marine Ecosystems.
2016,
Pubmed
Enomoto,
Microbial communities associated with holothurians: presence of unique bacteria in the coelomic fluid.
2012,
Pubmed
,
Echinobase
Fan,
Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress.
2013,
Pubmed
Felsenstein,
Evolutionary trees from DNA sequences: a maximum likelihood approach.
1981,
Pubmed
Frias-Lopez,
Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces.
2002,
Pubmed
Gottlieb,
Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies.
2008,
Pubmed
Hakim,
An abundance of Epsilonproteobacteria revealed in the gut microbiome of the laboratory cultured sea urchin, Lytechinus variegatus.
2015,
Pubmed
,
Echinobase
Hall,
The crown-of-thorns starfish genome as a guide for biocontrol of this coral reef pest.
2017,
Pubmed
,
Echinobase
Ho,
Arcobacter, what is known and unknown about a potential foodborne zoonotic agent!
2006,
Pubmed
Huson,
Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks.
2012,
Pubmed
Katharios,
Environmental marine pathogen isolation using mesocosm culture of sharpsnout seabream: striking genomic and morphological features of novel Endozoicomonas sp.
2015,
Pubmed
Kelly,
The Incidence and Morphology of Subcuticular Bacteria in the Echinoderm Fauna of New Zealand.
1995,
Pubmed
,
Echinobase
Kiselev,
Involvement of the cell-specific pigment genes pks and sult in bacterial defense response of sea urchins Strongylocentrotus intermedius.
2013,
Pubmed
,
Echinobase
Lawrence,
Subcuticular bacteria associated with two common New Zealand echinoderms: Characterization using 16S rRNA sequence analysis and fluorescence in situ hybridization.
2010,
Pubmed
,
Echinobase
Lee,
Kistimonas scapharcae sp. nov., isolated from a dead ark clam (Scapharca broughtonii), and emended description of the genus Kistimonas.
2012,
Pubmed
Lo,
Winding paths to simplicity: genome evolution in facultative insect symbionts.
2016,
Pubmed
Luo,
Pseudoalteromonas xishaensis sp. nov., isolated from Acanthaster planci in the Xisha islands.
2013,
Pubmed
,
Echinobase
Luter,
Microbiome analysis of a disease affecting the deep-sea sponge Geodia barretti.
2017,
Pubmed
McDonald,
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea.
2012,
Pubmed
McFall-Ngai,
Animals in a bacterial world, a new imperative for the life sciences.
2013,
Pubmed
Mendoza,
A novel agent (Endozoicomonas elysicola) responsible for epitheliocystis in cobia Rachycentrum canadum larvae.
2013,
Pubmed
Mortzfeld,
Response of bacterial colonization in Nematostella vectensis to development, environment and biogeography.
2016,
Pubmed
Nakagawa,
Microbiota in the coelomic fluid of two common coastal starfish species and characterization of an abundant Helicobacter-related taxon.
2017,
Pubmed
,
Echinobase
Neave,
Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas.
2016,
Pubmed
Neave,
Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts.
2017,
Pubmed
Nunan,
Spiroplasma penaei sp. nov., associated with mortalities in Penaeus vannamei, Pacific white shrimp.
2005,
Pubmed
Nunan,
Characterization and molecular methods for detection of a novel spiroplasma pathogenic to Penaeus vannamei.
2004,
Pubmed
Rajilić-Stojanović,
Diversity of the human gastrointestinal tract microbiota revisited.
2007,
Pubmed
Reed,
Skin and soft-tissue infections after injury in the ocean: culture methods and antibiotic therapy for marine bacteria.
1999,
Pubmed
,
Echinobase
Rivera-Posada,
Injection of Acanthaster planci with thiosulfate-citrate-bile-sucrose agar (TCBS). I. Disease induction.
2011,
Pubmed
,
Echinobase
Rivera-Posada,
Refined identification of Vibrio bacterial flora from Acanthasther planci based on biochemical profiling and analysis of housekeeping genes.
2011,
Pubmed
,
Echinobase
Schloss,
Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.
2009,
Pubmed
Schmieder,
Quality control and preprocessing of metagenomic datasets.
2011,
Pubmed
Slaby,
Metagenomic binning of a marine sponge microbiome reveals unity in defense but metabolic specialization.
2017,
Pubmed
Smith,
Echinoderm immunity.
2010,
Pubmed
,
Echinobase
Sunagawa,
Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata.
2009,
Pubmed
Tully,
Spiroplasma ixodetis sp. nov., a new species from Ixodes pacificus ticks collected in Oregon.
1995,
Pubmed
van de Water,
Spirochaetes dominate the microbial community associated with the red coral Corallium rubrum on a broad geographic scale.
2016,
Pubmed
Viver,
The low diverse gastric microbiome of the jellyfish Cotylorhiza tuberculata is dominated by four novel taxa.
2017,
Pubmed
Wang,
Spiroplasma eriocheiris sp. nov., associated with mortality in the Chinese mitten crab, Eriocheir sinensis.
2011,
Pubmed
Wang,
A spiroplasma associated with tremor disease in the Chinese mitten crab (Eriocheir sinensis).
2004,
Pubmed
Webster,
Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification.
2016,
Pubmed
,
Echinobase
Wessels,
The microbiome of the octocoral Lobophytum pauciflorum: minor differences between sexes and resilience to short-term stress.
2017,
Pubmed
Williamson,
Spiroplasma platyhelix sp. nov., a new mollicute with unusual morphology and genome size from the dragonfly Pachydiplax longipennis.
1997,
Pubmed
Wu,
WebMGA: a customizable web server for fast metagenomic sequence analysis.
2011,
Pubmed
Yang,
Estimating the pattern of nucleotide substitution.
1994,
Pubmed
Zbinden,
Occurrence of Deferribacterales and Entomoplasmatales in the deep-sea Alvinocarid shrimp Rimicaris exoculata gut.
2003,
Pubmed