Cold-Active Shewanella glacialimarina TZS-4T nov. Features a Temperature-Dependent Fatty Acid Profile and Putative Sialic Acid Metabolism

Muhammad Suleman Qasim; Mirka Lampi; Minna-Maria K Heinonen; Berta Garrido-Zabala; Dennis H Bamford; Reijo Käkelä; Elina Roine; Leif Peter Sarin

doi:10.3389/fmicb.2021.737641

Cold-Active Shewanella glacialimarina TZS-4_T nov. Features a Temperature-Dependent Fatty Acid Profile and Putative Sialic Acid Metabolism

Front Microbiol. 2021 Oct 1:12:737641. doi: 10.3389/fmicb.2021.737641. eCollection 2021.

Authors

Muhammad Suleman Qasim^{1

2}, Mirka Lampi¹, Minna-Maria K Heinonen¹, Berta Garrido-Zabala¹, Dennis H Bamford³, Reijo Käkelä^{3

4}, Elina Roine^{3

5}, Leif Peter Sarin¹

Affiliations

¹ RNAcious Laboratory, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland.
² Doctoral Programme in Microbiology and Biotechnology, University of Helsinki, Helsinki, Finland.
³ Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland.
⁴ Helsinki University Lipidomics Unit HiLIPID, Helsinki Institute of Life Science HiLIFE and Biocenter Finland, Helsinki, Finland.
⁵ The Laboratory of Structural Biology, Helsinki Institute of Life Science HiLIFE, Helsinki, Finland.

Abstract

Species of genus Shewanella are among the most frequently identified psychrotrophic bacteria. Here, we have studied the cellular properties, growth dynamics, and stress conditions of cold-active Shewanella strain #4, which was previously isolated from Baltic Sea ice. The cells are rod-shaped of ~2μm in length and 0.5μm in diameter, and they grow between 0 and 25°C, with an optimum at 15°C. The bacterium grows at a wide range of conditions, including 0.5-5.5% w/v NaCl (optimum 0.5-2% w/v NaCl), pH 5.5-10 (optimum pH 7.0), and up to 1mM hydrogen peroxide. In keeping with its adaptation to cold habitats, some polyunsaturated fatty acids, such as stearidonic acid (18:4n-3), eicosatetraenoic acid (20:4n-3), and eicosapentaenoic acid (20:5n-3), are produced at a higher level at low temperature. The genome is 4,456kb in size and has a GC content of 41.12%. Uniquely, strain #4 possesses genes for sialic acid metabolism and utilizes N-acetyl neuraminic acid as a carbon source. Interestingly, it also encodes for cytochrome c3 genes, which are known to facilitate environmental adaptation, including elevated temperatures and exposure to UV radiation. Phylogenetic analysis based on a consensus sequence of the seven 16S rRNA genes indicated that strain #4 belongs to genus Shewanella, closely associated with Shewanella aestuarii with a ~97% similarity, but with a low DNA-DNA hybridization (DDH) level of ~21%. However, average nucleotide identity (ANI) analysis defines strain #4 as a separate Shewanella species (ANI score=76). Further phylogenetic analysis based on the 92 most conserved genes places Shewanella strain #4 into a distinct phylogenetic clade with other cold-active marine Shewanella species. Considering the phylogenetic, phenotypic, and molecular characterization, we conclude that Shewanella strain #4 is a novel species and name it Shewanella glacialimarina sp. nov. TZS-4_T, where glacialimarina means sea ice. Consequently, S. glacialimarina TZS-4_T constitutes a promising model for studying transcriptional and translational regulation of cold-active metabolism.

Keywords: Shewanella; cold-active bacteria; polyunsaturated (essential) fatty acids; sea ice; sialic acid metabolism.