Genomic Analysis Reveals Adaptation of Vibrio campbellii to the Hadal Ocean

The genus Vibrio is characterized by high metabolic flexibility and genome plasticity and is widely distributed in the ocean from euphotic layers to deep-sea environments. The relationship between genome features and environmental adaptation strategies of Vibrio has been extensively investigated in coastal environments, yet very little is known about their survival strategies in oligotrophic deep-sea. In this study, we compared genomes of five Vibrio campbellii strains isolated from the Mariana and Yap Trenches at different water depths, including two epipelagic strains and three hadopelagic strains, to identify genomic characteristics that facilitate survival in the deep sea. Genome streamlining is found in pelagic strains, such as smaller genome sizes, lower G+C contents, and higher gene densities, which might be caused by long-term residence in an oligotrophic environment. Phylogenetic results showed that these five Vibrio strains are clustered into two clades according to their collection depth. Indeed, hadopelagic isolates harbor more genes involved in amino acid metabolism and transport, cell wall/membrane/envelope biogenesis, and inorganic ion transport and metabolism through comparative genomics analysis. Specific macrolide export gene and more tellurite resistance genes present in hadopelagic strains by the annotation of antibiotic and metal resistance genes. In addition, several genes related to substrate degradation are enriched in hadopelagic strains, such as chitinase genes, neopullulanase genes, and biopolymer transporter genes. In contrast, epipelagic strains are unique in their capacity for assimilatory nitrate reduction. The genomic characteristics investigated here provide insights into how Vibrio adapts to the deep-sea environment through genomic evolution. IMPORTANCE With the development of deep-sea sampling technology, an increasing number of deep-sea Vibrio strains have been isolated, but the adaptation mechanism of these eutrophic Vibrio strains to the deep-sea environment is unclear. Here, our results show that the genome of pelagic Vibrio is streamlined to adapt to a long-term oligotrophic environment. Through a phylogenomic analysis, we find that genomic changes in marine Vibrio campbellii strains are related to water depth. Our data suggest that an increase in genes related to antibiotic resistance, degradation of macromolecular and refractory substrates, and utilization of rare ions is related to the adaptation of V. campbellii strains to adapt to hadal environments, and most of the increased genes were acquired by horizontal gene transfer. These findings may deepen our understanding of adaptation strategies of marine bacteria to the extreme environment in hadal zones. With the development of deep-sea sampling technology, an increasing number of deep-sea Vibrio strains have been isolated, but the adaptation mechanism of these eutrophic Vibrio strains to the deep-sea environment is unclear. Here, our results show that the genome of pelagic Vibrio is streamlined to adapt to a long-term oligotrophic environment.

Automated summary

This study compared the genomes of five Vibrio campbellii strains isolated from different depths of the Mariana and Yap Trenches and identified genomic characteristics that facilitate survival in the deep sea. Pelagic strains showed genome streamlining, while deep-sea strains had more genes involved in amino acid metabolism, cell wall biogenesis, and ion transport and metabolism. Deep-sea strains also had specific antibiotic resistance and substrate degradation genes. In contrast, pelagic strains had the ability for assimilatory nitrate reduction.