Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
Sci Rep
2017 Aug 18;71:8764. doi: 10.1038/s41598-017-09355-2.
Show Gene links
Show Anatomy links
Microbiota in the coelomic fluid of two common coastal starfish species and characterization of an abundant Helicobacter-related taxon.
Nakagawa S
,
Saito H
,
Tame A
,
Hirai M
,
Yamaguchi H
,
Sunata T
,
Aida M
,
Muto H
,
Sawayama S
,
Takaki Y
.
???displayArticle.abstract???
Marine invertebrates associate with diverse microorganisms. Microorganisms even inhabit coelomic fluid (CF), namely, the fluid filling the main body cavity of echinoderms. The CF microbiota potentially impacts host health and disease. Here, we analysed the CF microbiota in two common coastal starfish species, Patiria pectinifera and Asterias amurensis. Although microbial community structures were highly variable among individual starfish, those of P. pectinifera were compositionally similar to those in the surrounding seawater. By contrast, many A. amurensis individuals harboured unique microbes in the CF, which was dominated by the unclassified Thiotrichales or previously unknown Helicobacter-related taxon. In some individuals, the Helicobacter-related taxon was the most abundant genus-level taxon, accounting for up to 97.3% of reads obtained from the CF microbial community. Fluorescence in situ hybridization using a Helicobacter-related-taxon-specific probe suggested that probe-reactive cells in A. amurensis were spiral-shaped, morphologically similar to known Helicobacter species. Electron microscopy revealed that the spiral cells had a prosthecate-like polar appendage that has never been reported in Helicobacter species. Although culture of Helicobacter-related taxon was unsuccessful, this is the first report of the dominance of a Helicobacter-related taxon in invertebrates and non-digestive organs, reshaping our knowledge of the phylogeography of Helicobacter-related taxa.
Figure 1. Histogram showing the relative abundance of 16S rRNA gene amplicon reads assigned to family level taxa in the various samples. UPGMA (Unweighted Pair Group Method with Arithmetic mean) clustering based on weighted UniFrac distances is also shown. Each colour on the graph represents a distinct family. Families with >10% relative abundance in any sample are presented, and the rest and unassigned taxa are indicated as ‘others’. The family Helicobacteraceae is divided into Helicobacter-related taxon and Helicobacter-unrelated taxa (mainly Sulfuricurvum, Sulfurimonas, and Sulfurovum relatives). Sample names represent sampling year, sampling site (N or H, Nemuro City; U or M, Hakodate City), starfish species (A. amurensis, M; P. pectinifera, I), body parts (CF, coelomic fluid; S, body surface) or seawater (SW), and individual number. “-Bulk†indicates bulk samples. A. amurensis, P. pectinifera, seawater, and starfish body surface samples are shown in red, blue, green, and black, respectively. Read numbers and ratios of Helicobacter-related taxon against bacteria estimated by quantitative PCR are shown in parentheses on right side of histograms. Detailed taxonomic information is provided in Supplementary Table 5.
Figure 2. Analysis of microbial communities using principal coordinate analysis (PCoA).
Figure 3. Phylogenetic tree of representative members of the genera Helicobacter and Wolinella inferred from 16S rRNA gene sequences by the neighbour joining method using 856 homologous sequence positions. The accession numbers are shown in parentheses. Bootstrap values (expressed as percentages of 1,000 replications) higher than 50% are shown at branching points. The sequence found in the CF of A. amurensis is shown in bold. The scale bar represents 0.01 substitutions per nucleotide position.
Figure 4. Epifluorescence micrograph of cells binding DAPI (A, blue) and the Helicobacter-related-taxon-specific probe (B, green) in the CF of A. amurensis (sample ID, 2015N-MCF-D). Bar, 5 µm.
Figure 5. Electron micrographs of the spiral cells found in the CF of A. amurensis (sample ID, 2015N-MCF-D). Transmission electron micrographs of negatively stained cells (A,B). Scanning electron micrographs (C,D). Magnified views of the polar cell appendage (B,D).
Baar,
Complete genome sequence and analysis of Wolinella succinogenes.
2003, Pubmed
Baar,
Complete genome sequence and analysis of Wolinella succinogenes.
2003,
Pubmed
Birkbeck,
Francisella infections in fish and shellfish.
2011,
Pubmed
Brevik,
Francisella halioticida sp. nov., a pathogen of farmed giant abalone (Haliotis gigantea) in Japan.
2011,
Pubmed
Caporaso,
QIIME allows analysis of high-throughput community sequencing data.
2010,
Pubmed
Carbone,
Occurrence of Helicobacter pylori DNA in the coastal environment of southern Italy (Straits of Messina).
2005,
Pubmed
Castro,
Vibrios isolated from the cultured manila clam (Ruditapes philippinarum): numerical taxonomy and antibacterial activities.
2002,
Pubmed
Clayton,
Sensitive detection of Helicobacter pylori by using polymerase chain reaction.
1992,
Pubmed
Collard,
Buffer capacity of the coelomic fluid in echinoderms.
2013,
Pubmed
,
Echinobase
Coteur,
Peptidoglycan recognition proteins with amidase activity in early deuterostomes (Echinodermata).
2007,
Pubmed
,
Echinobase
Coteur,
Differentiation of immune cells challenged by bacteria in the common European starfish, Asterias rubens (Echinodermata).
2002,
Pubmed
,
Echinobase
Coteur,
Increased phagocytic activity in contaminated seastars (Asterias rubens) collected in the Southern Bight of the North Sea.
2005,
Pubmed
,
Echinobase
Edgar,
Search and clustering orders of magnitude faster than BLAST.
2010,
Pubmed
Enomoto,
Microbial communities associated with holothurians: presence of unique bacteria in the coelomic fluid.
2012,
Pubmed
,
Echinobase
Foley,
Tularemia.
2010,
Pubmed
Fox,
Helicobacter marmotae sp. nov. isolated from livers of woodchucks and intestines of cats.
2002,
Pubmed
Fraune,
Host-specificity of environmentally transmitted Mycoplasma-like isopod symbionts.
2008,
Pubmed
Gajardo,
A high-resolution map of the gut microbiota in Atlantic salmon (Salmo salar): A basis for comparative gut microbial research.
2016,
Pubmed
Gatesoupe,
The highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, Dicentrarchus labrax, submitted to different nutritional histories.
2016,
Pubmed
Gilbert,
Occurrence, diversity, and host association of intestinal Campylobacter, Arcobacter, and Helicobacter in reptiles.
2014,
Pubmed
Hakim,
An abundance of Epsilonproteobacteria revealed in the gut microbiome of the laboratory cultured sea urchin, Lytechinus variegatus.
2015,
Pubmed
,
Echinobase
Hasegawa,
[A multicenter study of a new Helicobacter pylori selective medium. Columbia horse blood agar HP].
2002,
Pubmed
Haug,
Antibacterial activity in Strongylocentrotus droebachiensis (Echinoidea), Cucumaria frondosa (Holothuroidea), and Asterias rubens (Asteroidea).
2002,
Pubmed
,
Echinobase
Hewson,
Densovirus associated with sea-star wasting disease and mass mortality.
2014,
Pubmed
,
Echinobase
Huse,
Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing.
2008,
Pubmed
Langmead,
Fast gapped-read alignment with Bowtie 2.
2012,
Pubmed
Leclercq,
Phylogenomics of "Candidatus Hepatoplasma crinochetorum," a lineage of mollicutes associated with noninsect arthropods.
2014,
Pubmed
Lokmer,
Spatial and Temporal Dynamics of Pacific Oyster Hemolymph Microbiota across Multiple Scales.
2016,
Pubmed
Lokmer,
Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection.
2015,
Pubmed
Lozupone,
UniFrac: a new phylogenetic method for comparing microbial communities.
2005,
Pubmed
Ludwig,
ARB: a software environment for sequence data.
2004,
Pubmed
Matranga,
Monitoring chemical and physical stress using sea urchin immune cells.
2005,
Pubmed
,
Echinobase
Nakagawa,
Allying with armored snails: the complete genome of gammaproteobacterial endosymbiont.
2014,
Pubmed
Nakagawa,
Deep-sea vent epsilon-proteobacterial genomes provide insights into emergence of pathogens.
2007,
Pubmed
Nakagawa,
Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field.
2005,
Pubmed
Nakagawa,
Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance.
2008,
Pubmed
Olafsen,
Indigenous bacteria in hemolymph and tissues of marine bivalves at low temperatures.
1993,
Pubmed
Osbourn,
The saponins: polar isoprenoids with important and diverse biological activities.
2011,
Pubmed
,
Echinobase
Pérez-Matos,
Bacterial diversity associated with the Caribbean tunicate Ecteinascidia turbinata.
2007,
Pubmed
Pérez-Rodríguez,
From deep-sea volcanoes to human pathogens: a conserved quorum-sensing signal in Epsilonproteobacteria.
2015,
Pubmed
Pinsino,
Coelomocytes and post-traumatic response in the common sea star Asterias rubens.
2007,
Pubmed
,
Echinobase
Quast,
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools.
2013,
Pubmed
Schofield,
Identification and analysis of the bacterial endosymbiont specialized for production of the chemotherapeutic natural product ET-743.
2015,
Pubmed
Shen,
Helicobacter rodentium sp. nov., a urease-negative Helicobacter species isolated from laboratory mice.
1997,
Pubmed
Solnick,
Emergence of diverse Helicobacter species in the pathogenesis of gastric and enterohepatic diseases.
2001,
Pubmed
Takai,
Spatial distribution of marine crenarchaeota group I in the vicinity of deep-sea hydrothermal systems.
2004,
Pubmed
Twing,
Temporal study of Helicobacter pylori presence in coastal freshwater, estuary and marine waters.
2011,
Pubmed
Wallner,
Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms.
1993,
Pubmed
Wang,
A shrimp C-type lectin inhibits proliferation of the hemolymph microbiota by maintaining the expression of antimicrobial peptides.
2014,
Pubmed
Wang,
Bacterial symbionts in the hepatopancreas of isopods: diversity and environmental transmission.
2007,
Pubmed
Wang,
Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy.
2007,
Pubmed
Watanabe,
Design and evaluation of PCR primers to amplify bacterial 16S ribosomal DNA fragments used for community fingerprinting.
2001,
Pubmed
Wong,
Aquacultured rainbow trout (Oncorhynchus mykiss) possess a large core intestinal microbiota that is resistant to variation in diet and rearing density.
2013,
Pubmed
Yamaoka,
Relationship of vacA genotypes of Helicobacter pylori to cagA status, cytotoxin production, and clinical outcome.
1998,
Pubmed
Yamazaki,
Individual Apostichopus japonicus fecal microbiome reveals a link with polyhydroxybutyrate producers in host growth gaps.
2016,
Pubmed
,
Echinobase
Yilmaz,
mathFISH, a web tool that uses thermodynamics-based mathematical models for in silico evaluation of oligonucleotide probes for fluorescence in situ hybridization.
2011,
Pubmed
Zhang,
PEAR: a fast and accurate Illumina Paired-End reAd mergeR.
2014,
Pubmed
Zhang,
Pseudoruegeria marinistellae sp. nov., isolated from an unidentified starfish in Sanya, China.
2017,
Pubmed
,
Echinobase
