Comprehensive Genomic Characterization of Marine Bacteria Thalassospira spp. Provides Insights into Their Ecological Roles in Aromatic Hydrocarbon-Exposed Environments

The marine bacterial genus Thalassospira has often been identified as an abundant member of polycyclic aromatic hydrocarbon (PAH)-exposed microbial communities. However, despite their potential usability for biotechnological applications, functional genes that are conserved in their genomes have barely been investigated. Thus, the goal of this study was to comprehensively examine the functional genes that were potentially responsible for aromatic hydrocarbon biodegradation in the Thalassospira genomes available from databases, including a new isolate of Thalassospira, strain GO-4, isolated from a phenanthrene-enriched marine bacterial consortium. Strain GO-4 was used in this study as a model organism to link the genomic data and their metabolic functions. Strain GO-4 growth assays confirmed that it utilized a common phenanthrene biodegradation intermediate 2-carboxybenzaldehyde (CBA) as the sole source of carbon and energy, but did not utilize phenanthrene. Consistently, strain GO-4 was found to possess homologous genes of phdK, pht, and pca that encode enzymes for biodegradation of CBA, phthalic acid, and protocatechuic acid, respectively. Further comprehensive genomic analyses for 33 Thalassospira genomes from databases showed that a gene cluster that consisted of phdK and pht homologs was conserved in 13 of the 33 strains. pca gene homologs were found in all examined genomes; however, homologs of the known PAH-degrading genes, such as the pah, phn, or nah genes, were not found. Possibly Thalassospira spp. co-occupy niches with other PAH-degrading bacteria that provide them with PAH degradation intermediates and facilitated their inhabitation in PAH-exposed microbial ecosystems. IMPORTANCE Comprehensive investigation of multiple genomic data sets from targeted microbial taxa deposited in databases may provide substantial information to predict metabolic capabilities and ecological roles in different environments. This study is the first report that details the functional profiling of Thalassospira spp. that have repeatedly been found in polycyclic aromatic hydrocarbon (PAH)-exposed marine bacterial communities by using genomic data from a new isolate, Thalassospira strain GO-4, and other strains in databases. Through screening of functional genes potentially involved in aromatic hydrocarbon biodegradation across 33 Thalassospira genomes and growth assays for strain GO-4, it was suggested that Thalassospira spp. unexceptionally conserved the ability to metabolize single-ring, PAH biodegradation intermediates, while being incapable of utilizing PAHs. This expanded our understanding of this potentially important contributing member to PAH-degrading microbial ecosystems; such species are considered to be specialized in driving downstream reactions of PAH biodegradation.