Genome sequence of the deep-sea gamma-proteobacterium Idiomarina loihiensis reveals amino acid fermentation as a source of carbon and energy

Abstract

We report the complete genome sequence of the deep-sea gamma-proteobacterium, Idiomarina loihiensis, isolated recently from a hydrothermal vent at 1,300-m depth on the Loihi submarine volcano, Hawaii. The I. loihiensis genome comprises a single chromosome of 2,839,318 base pairs, encoding 2,640 proteins, four rRNA operons, and 56 tRNA genes. A comparison of I. loihiensis to the genomes of other gamma-proteobacteria reveals abundance of amino acid transport and degradation enzymes, but a loss of sugar transport systems and certain enzymes of sugar metabolism. This finding suggests that I. loihiensis relies primarily on amino acid catabolism, rather than on sugar fermentation, for carbon and energy. Enzymes for biosynthesis of purines, pyrimidines, the majority of amino acids, and coenzymes are encoded in the genome, but biosynthetic pathways for Leu, Ile, Val, Thr, and Met are incomplete. Auxotrophy for Val and Thr was confirmed by in vivo experiments. The I. loihiensis genome contains a cluster of 32 genes encoding enzymes for exopolysaccharide and capsular polysaccharide synthesis. It also encodes diverse peptidases, a variety of peptide and amino acid uptake systems, and versatile signal transduction machinery. We propose that the source of amino acids for I. loihiensis growth are the proteinaceous particles present in the deep sea hydrothermal vent waters. I. loihiensis would colonize these particles by using the secreted exopolysaccharide, digest these proteins, and metabolize the resulting peptides and amino acids. In summary, the I. loihiensis genome reveals an integrated mechanism of metabolic adaptation to the constantly changing deep-sea hydrothermal ecosystem.

Fig. 1.

Circular representation of the I. loihiensis genome. From the outside inward: The first and second circles show predicted gene-coding region in plus and minus strands, respectively. By COG functional categories, red indicates translation, ribosomal structure, and biogenesis; blue indicates transcription; pink indicates DNA replication, recombination, and repair; green indicates cell division and chromosome partitioning; dark red indicates posttranslational modification; orange indicates cell envelope biogenesis, outer membrane; navy blue indicates cell motility and secretion; purple indicates inorganic ion transport and metabolism; wheat indicates signal transduction mechanisms; aquamarine indicates energy production and conversion; beige indicates carbohydrate transport and metabolism; blue-violet indicates amino acid transport and metabolism; light sky blue indicates nucleotide transport and metabolism; gold indicates coenzyme metabolism; dark khaki indicates lipid metabolism; magenta indicates secondary metabolites biosynthesis; light cyan indicates, general function prediction only; gray indicates function unknown; black indicates hypothetical. The third circle shows transposons and insertion sequence elements in red. The fourth circle shows pseudogenes in brown. The fifth and sixth circles show tRNAs and rRNAs in olive and dark green respectively.

Fig. 2.

Phylogenetic position of I. loihiensis. Maximum likelihood phylogenetic tree of γ-Proteobacteria constructed from concatenated alignments of ribosomal proteins. Circles indicate internal nodes with resampling of estimated log-likelihoods (RELL) bootstrap support >95%. Distances are indicated in substitutions per site.

Fig. 3.

Comparative genomic analysis of I. loihiensis proteins. (A) Phylogenetic distribution of the closest homologs of I. loihiensis proteins. The numbers indicate (in the clockwise order) best hits among γ-proteobacteria (77%), other proteobacteria, firmicutes, cyanobacteria, other organisms, and proteins with no homologs. (B) Functional distribution of I. loihiensis proteins. The columns indicate the number of protein families (COGs) encoded in the genomes of seven free-living γ-proteobacteria (E. coli K12, E. coli O157:H7, Salmonella typhimurium, Yersinia pestis, V. cholerae, and Pseudomonas aeruginosa), but not in I. loihiensis (Bottom); those shared by I. loihiensis and seven other γ-proteobacteria (Middle); and those found in I. loihiensis but not in any of the others (Top). Protein functional groups represent translation (J), replication, recombination and repair (L), energy production and conversion (C), and transport and metabolism of amino acids (E), carbohydrates (G), nucleotides (F), coenzymes (H), lipids (I), and inorganic ions (P).

Fig. 4.

A scheme of the principal functional systems of the I. loihiensis cell. I. loihiensis gene identifiers are shown by numbers in green. Pathways involving multiple reactions shown by double arrows. Final biosynthetic products are indicated as follows: light blue for amino acids, dark yellow for nucleotides, brown for sugars, and red for cofactors. Reactions for which no candidate enzyme was confidently identified are indicated by question marks. Missing reactions of Thr and Val biosynthesis are crossed out; the uptake of these two essential amino acids is indicated with exclamation points.

Fig. 5.

A schematic diagram of lifestyle of I. loihiensis inferred from genome analysis.