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Sci Rep
2017 Aug 18;71:8764. doi: 10.1038/s41598-017-09355-2.
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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
.
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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).
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