Metabolic Versatility of the Family Halieaceae Revealed by the Genomics of Novel Cultured Isolates

The family Halieaceae (OM60/NOR5 clade) is a gammaproteobacterial group abundant and cosmopolitan in coastal seawaters and plays an important role in response to phytoplankton blooms. However, the ecophysiology of this family remains understudied because of the vast gap between phylogenetic diversity and cultured representatives. Here, using six pure cultured strains isolated from coastal seawaters, we performed in-depth genomic analyses to provide an overview of the phylogeny and metabolic capabilities of this family. The combined analyses of 16S rRNA genes, genome sequences, and functional genes relevant to taxonomy demonstrated that each strain represents a novel species. Notably, two strains belonged to the hitherto-uncultured NOR5-4 and NOR5-12 subclades. Metabolic reconstructions revealed that the six strains likely have aerobic chemo- or photoheterotrophic lifestyles; five of them possess genes for proteorhodopsin or aerobic anoxygenic phototrophy. The presence of blue- or green-tuned proteorhodopsin in Halieaceae suggested their ability to adapt to light conditions varying with depth or coastal-to-open ocean transition. In addition to the genes of anaplerotic CO(2) fixation, genes encoding a complete reductive glycine pathway for CO(2) fixation were found in three strains. Putative polysaccharide utilization loci were detected in three strains, suggesting the association with phytoplankton blooms. Read mapping of various metagenomes and metatranscriptomes showed that the six strains are widely distributed and transcriptionally active in marine environments. Overall, the six strains genomically characterized in this study expand the phylogenetic and metabolic diversity of Halieaceae and likely serve as a culture resource for investigating the ecophysiological features of this environmentally relevant bacterial group. IMPORTANCE Although the family Halieaceae (OM60/NOR5 clade) is an abundant and cosmopolitan clade widely found in coastal seas and involved in interactions with phytoplankton, a limited number of cultured isolates are available. In this study, we isolated six pure cultured Halieaceae strains from coastal seawaters and performed a comparative physiological and genomic analysis to give insights into the phylogeny and metabolic potential of this family. The cultured strains exhibited diverse metabolic potential by harboring genes for anaplerotic CO(2) fixation, proteorhodopsin, and aerobic anoxygenic phototrophy. Polysaccharide utilization loci detected in some of these strains also indicated an association with phytoplankton blooms. The cultivation of novel strains of Halieaceae and their genomic characteristics largely expanded the phylogenetic and metabolic diversity, which is important for future ecophysiological studies.