Abstract
Shewanella baltica was the dominant culturable nitrate-reducing bacterium in the eutrophic and strongly stratified Baltic Sea in the 1980s, where it primarily inhabited the oxic-anoxic transition zone. The genomic structures of 46 of these isolates were investigated through comparative genomic hybridization (CGH), which revealed a gradient of genomic similarity, ranging from 65% to as high as 99%. The core genome of the S. baltica species was enriched in anaerobic respiration-associated genes. Auxiliary genes, most of which locate within a few genomic islands (GIs), were nonuniformly distributed among the isolates. Specifically, hypothetical and mobile genetic element (MGE)-associated genes dominated intraclade gene content differences, whereas gain/loss of functional genes drove gene content differences among less related strains. Among the major S. baltica clades, gene signatures related to specific redox-driven and spatial niches within the water column were identified. For instance, genes involved in anaerobic respiration of sulfur compounds may provide key adaptive advantages for clade A strains in anoxic waters where sulfur-containing electron acceptors are present. Genes involved in cell motility, in particular, a secondary flagellar biosynthesis system, may be associated with the free-living lifestyle by clade E strains. Collectively, this study revealed characteristics of genome variations present in the water column and active speciation of S. baltica strains, driven by niche partitioning and horizontal gene transfer (HGT).IMPORTANCE Speciation in nature is a fundamental process driving the formation of the vast microbial diversity on Earth. In the central Baltic Sea, the long-term stratification of water led to formation of a large-scale vertical redoxcline that provided a gradient of environmental niches with respect to the availability of electron acceptors and donors. The region was home to Shewanella baltica populations, which composed the dominant culturable nitrate-reducing bacteria, particularly in the oxic-anoxic transition zone. Using the collection of S. baltica isolates as a model system, genomic variations showed contrasting gene-sharing patterns within versus among S. baltica clades and revealed genomic signatures of S. baltica clades related to redox niche specialization as well as particle association. This study provides important insights into genomic mechanisms underlying bacterial speciation within this unique natural redoxcline.
Highlights
Shewanella baltica was the dominant culturable nitrate-reducing bacterium in the eutrophic and strongly stratified Baltic Sea in the 1980s, where it primarily inhabited the oxic-anoxic transition zone
We explored the genomic variations in a set of Shewanella baltica strains isolated from the stratified basin in the central Baltic Sea during 1986 to 1987 and in 1998 [12,13,14]
Compared to the auxiliary genes, the S. baltica core genome is enriched in genes involved in central metabolism, including those associated with transport and metabolism of coenzymes, amino acids, and nucleotides; translation; signal transduction; ribosomal structure and biogenesis; and posttranslational modification as well as energy production and conversion
Summary
Shewanella baltica was the dominant culturable nitrate-reducing bacterium in the eutrophic and strongly stratified Baltic Sea in the 1980s, where it primarily inhabited the oxic-anoxic transition zone. We explored the genomic variations in a set of Shewanella baltica strains isolated from the stratified basin in the central Baltic Sea during 1986 to 1987 and in 1998 [12,13,14]. These S. baltica strains were obtained through attempts to isolate nitrate-reducing bacteria in the eutrophicated Baltic Sea waters at both Gotland Deep station and Station T. Clade A strains were recovered only from Gotland Deep station with the presence of hydrogen sulfide in deep anoxic water They were favorably isolated using thiosulfate-containing medium under anaerobic culture conditions, representing a group of “sulfur specialists” within S. baltica. Together with other S. baltica clades, these strains formed an intraspecific gradient of genetic relatedness and provided a msystems.asm.org 2
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