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. 2024 Apr;16(2):e13238.
doi: 10.1111/1758-2229.13238.

Functional analyses of bacterial genomes found in Symbiodiniaceae genome assemblies

Eiichi Shoguchi  1 , Masanobu Kawachi  2 , Chuya Shinzato  3 , Girish Beedessee  1   4
Affiliations

Functional analyses of bacterial genomes found in Symbiodiniaceae genome assemblies

Eiichi Shoguchi et al. Environ Microbiol Rep. 2024 Apr.

Abstract

Bacterial-algal interactions strongly influence marine ecosystems. Bacterial communities in cultured dinoflagellates of the family Symbiodiniaceae have been characterized by metagenomics. However, little is known about whole-genome analysis of marine bacteria associated with these dinoflagellates. We performed in silico analysis of four bacterial genomes from cultures of four dinoflagellates of the genera Symbiodinium, Breviolum, Cladocopium and Durusdinium. Comparative analysis showed that the former three contain the alphaproteobacterial family Parvibaculaceae and that the Durusdinium culture includes the family Sphingomonadaceae. There were no large genomic reductions in the alphaproteobacteria with genome sizes of 2.9-3.9 Mb, implying they are not obligate intracellular bacteria. Genomic annotations of three Parvibaculaceae detected the gene for diacetylchitobiose deacetylase (Dac), which may be involved in the degradation of dinoflagellate cell surfaces. They also had metabolic genes for dissimilatory nitrate reduction to ammonium (DNRA) in the nitrogen (N) cycle and cobalamin (vitamin B12 ) biosynthetic genes in the salvage pathway. Those three characters were not found in the Sphingomonadaceae genome. Predicted biosynthetic gene clusters for secondary metabolites indicated that the Parvibaculaceae likely produce the same secondary metabolites. Our study suggests that the Parvibaculaceae is a major resident of Symbiodiniaceae cultures with antibiotics.

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Conflict of interest statement

The authors have no conflict of interest to declare.

Figures

FIGURE 1
FIGURE 1
Genomic characterization of dinoflagellate‐associated bacteria. (A) White colonies with red arrows indicate isolated alphaproteobacterial Parvibaculaceae in Cladocopium (Symbiodiniaceae) on an agar plate. Scale bar: 1 mm. (B) Live bacterial cells from a white colony were confirmed and photographed under differential interference contrast (DIC) microscopy using a Zeiss AxioImager Z1 microscope equipped with an AxioCam digital camera (Zeiss, Jena, Germany). Cell lengths were less than 10 μm, and cell images with arrowheads are likely to be from multiple cells. Scale bar: 10 μm. (C) The classification of analysed genomes with the Genome Taxonomy Database. A part of the molecular phylogenetic tree is shown (see Figure S4 for the entire phylogenetic tree). (D) Circular plots of the 3.9‐Mb alphaproteobacterial Parvibaculaceae Y103 genome. The outermost circle (orange circle (1) shows predicted coding sequences on the forward strand. Green and purple in circle 2 indicate plus and minus GC skews, respectively. The black waveform circle 3 shows GC content. The innermost circle (orange circle 4) shows predicted coding sequences on the reverse strand. tRNA, tmRNA (transfer‐messenger RNA) and rRNA genes are shown in blue, green and red letters, respectively. (E) Venn diagrams of gene content of analysed alphaproteobacterial genomes. (F) Inferred metabolism from decoded alphaproteobacterial genomes (blue‐highlighted). Potential metabolites of four Symbiodiniaceae‐associated bacteria were predicted using Prokka annotations. Annotations for 22 other genomes are shown for comparison (Tables 1 and S1). Three metabolic pathways surrounded with blue lines are found in three Parvibaculaceae genomes, but not that of Sphingomonadaceae.
FIGURE 2
FIGURE 2
Putative biosynthetic genes for secondary metabolites from genomes of major dinoflagellate‐associated bacteria. (A) Biosynthetic pathways of vitamin B12 and putative enzymatic genes show that salvage pathways biosynthesize adenosylcobalamin in Parvibaculaceae P.Y106 and P.Y103. (B) Putative biosynthetic gene clusters in genomes of Symbiodiniaceae‐associated bacteria (P.Y103 and S.NIES‐2907). More than 80% of genes in clusters, except the lasso peptide biosynthetic gene cluster (region 2 in NIES‐2907), showed similarities to clustered genes in known bacterial genomes (see Figure S6). Predicted links between gene clusters and secondary metabolites are shown by the numbers in parentheses.
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