Genomic and phenotypic characterization of 26 novel marine bacterial strains with relevant biogeochemical roles and widespread presence across the global ocean

Abstract

Prokaryotes dominate global oceans and shape biogeochemical cycles, yet most taxa remain uncultured and uncharacterized as of today. Here we present the characterization of 26 novel marine bacterial strains from a large isolate collection obtained from Blanes Bay (NW Mediterranean) microcosm experiments made in the four seasons. Morphological, cultural, biochemical, physiological, nutritional, genomic, and phylogenomic analyses were used to characterize and phylogenetically place the novel isolates. The strains represent 23 novel bacterial species and six novel genera: three novel species pertaining to class Alphaproteobacteria (families Rhodobacteraceae and Sphingomonadaceae), six novel species and three new genera from class Gammaproteobacteria (families Algiphilaceae, Salinispheraceae, and Alteromonadaceae), 13 novel species and three novel genera from class Bacteroidia (family Flavobacteriaceae), and one new species from class Rhodothermia (family Rubricoccaceae). The bacteria described here have potentially relevant roles in the cycles of carbon (e.g., carbon fixation or energy production via proteorhodopsin), nitrogen (e.g., denitrification or use of urea), sulfur (oxidation of sulfur compounds), phosphorus (acquisition and use of different forms of phosphorus and remodeling of membrane phospholipids), and hydrogen (oxidation of hydrogen to obtain energy). We mapped the genomes of the presented strains to the Tara Oceans metagenomes to reveal that these strains were globally distributed, with those of the family Flavobacteriaceae being the most widespread and abundant, while Rhodothermia being the rarest and most localized. While molecular-only approaches are also important, our study stresses the importance of culturing as a powerful tool to further understand the functioning of marine bacterial communities.

Keywords: biogeochemistry; biogeography; genomics; isolates; marine bacteria; phylogenomics; taxonomy.

Figure 1

Phylogenomic tree generated with UBCG2 (Kim J, et al., 2021) of the strains belonging to the class Alphaproteobacteria and their closest neighbors according to the TYGS (Type Strain Genome Server). The strains characterized in this study are highlighted in bold. Accession numbers for these genomes can be found in Supplementary Table S5. The numbers at the nodes indicate the gene support index, with 81 being the maximum value.

Figure 2

Phylogenomic tree generated with UBCG2 (Kim J, et al., 2021) of the strains belonging to the class Gammaproteobacteria and their closest neighbors according to the TYGS (Type Strain Genome Server). The strains characterized in this study are highlighted in bold. Accession numbers for these genomes can be found in Supplementary Table S5. The numbers at the nodes indicate the gene support index, with 81 being the maximum value.

Figure 3

Phylogenomic tree generated with UBCG2 (Kim J, et al., 2021) of the strains belonging to the family Flavobacteriaceae and their closest neighbors according to the TYGS (Type Strain Genome Server). The strains characterized in this study are highlighted in bold. Accession numbers for these genomes can be found in Supplementary Table S5. The numbers at the nodes indicate the gene support index, with 81 being the maximum value.

Figure 4

Phylogenomic tree generated with UBCG2 (Kim J, et al., 2021) of the strains belonging to the class Rhodothermia and their closest neighbors according to the TYGS (Type Strain Genome Server). The strains characterized in this study are highlighted in bold. Accession numbers for these genomes can be found in Supplementary Table S5. The numbers at the nodes indicate the gene support index, with 81 being the maximum value.

Figure 5

Heatmap indicating the presence/absence of genes relevant to biogeochemical cycles among the novel genomes. Only the genes with at least one positive value are shown.

Figure 6

Heatmap indicating the abundance of the described strains in different oceans and layers. The gray color indicates absence, and the white color indicates no data. Data obtained by mapping the genomes to the Tara Oceans metagenomes. SRF, surface; MES, mesopelagic.

Figure 7

Geographic distribution of the presented strains grouped by class, taking into account different ocean layers. Data matched to the Tara Oceans metagenomes. SRF, surface; DCM, deep chlorophyll maximum; MES, mesopelagic.