Ice-Binding Proteins Associated with an Antarctic Cyanobacterium, Nostoc sp. HG1

• Published in: Applied and environmental microbiology Vol. 87; no. 2; pp. 1 - 12
• Main Authors: Raymond, James A, Janech, Michael G, Mangiagalli, Marco
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 04.01.2021
• Subjects: Algae; Amino acid sequence; Amino acids; Antarctic Regions; Bacteria; Bacterial Proteins - chemistry; Bacterial Proteins - genetics; Binding; Carrier Proteins - chemistry; Carrier Proteins - genetics; Cell membranes; Circular dichroism; Cyanobacteria; Deoxyribonucleic acid; Dichroism; DNA; Environmental Microbiology; Ice; Mass spectrometry; Mass spectroscopy; Metagenome; Nostoc; Nostoc - genetics; Nucleotide sequence; Nucleotides; Polar environments; Protein structure; Proteins; Proteomics; Secondary structure; Antarctic Regions; Antarctica; Nostoc; PEP C-terminal signal; ice-binding proteins; horizontal gene transfer
• ISSN: 0099-2240; 1098-5336
• DOI: 10.1128/AEM.02499-20

Ice-binding proteins (IBPs) have been identified in numerous polar algae and bacteria, but so far not in any cyanobacteria, despite the abundance of cyanobacteria in polar regions. We previously reported strong IBP activity associated with an Antarctic species. In this study, to identify the proteins responsible, as well as elucidate their origin, we sequenced the DNA of an environmental sample of this species, designated sp. HG1, and its bacterial community and attempted to identify IBPs by looking for known IBPs in the metagenome and by looking for novel IBPs by tandem mass spectrometry (MS/MS) proteomics analyses of ice affinity-purified proteins. The metagenome contained over 116 DUF3494-type IBP genes, the most common type of IBP identified so far. One of the IBPs could be confidently assigned to , while the others could be attributed to diverse bacteria, which, surprisingly, accounted for the great majority of the metagenome. Recombinant IBPs (nIBPs) had strong ice-structuring activities, and their circular dichroism spectra were consistent with the secondary structure of a DUF3494-type IBP. nIBP is unusual in that it is the only IBP identified so far to have a PEP (amino acid motif) C-terminal signal, a signal that has been associated with anchoring to the outer cell membrane. These results suggest that the observed IBP activity of sp. HG1 was due to a combination of endogenous and exogenous IBPs. Amino acid and nucleotide sequence analyses of nIBP raise the possibility that it was acquired from a planctomycete. The horizontal transfer of genes encoding ice-binding proteins (IBPs), proteins that confer freeze-thaw tolerance, has allowed many microorganisms to expand their ranges into polar regions. One group of microorganisms for which nothing is known about its IBPs is cyanobacteria. In this study, we identified a cyanobacterial IBP and showed that it was likely acquired from another bacterium, probably a planctomycete. We also showed that a consortium of IBP-producing bacteria living with the contribute to its IBP activity.