Ice‐binding proteins from the fungus Antarctomyces psychrotrophicus possibly originate from two different bacteria through horizontal gene transfer

• Published in: The FEBS journal 2019-03, Vol.286 (5), p.946-962
• Main Authors: Arai, Tatsuya, Fukami, Daichi, Hoshino, Tamotsu, Kondo, Hidemasa, Tsuda, Sakae
• Format: Article
• Language: English
• Subjects: Amino Acid Sequence; Antifreeze Proteins - chemistry; Antifreeze Proteins - genetics; Antifreeze Proteins - metabolism; ascomycete; Ascomycota; Ascomycota - metabolism; Bacteria; Bacteria - classification; Bacteria - metabolism; Bacterial Proteins - chemistry; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Binding; Evolution & development; freeze resistance; Freeze-thawing; Freezing; Fungal Proteins - chemistry; Fungal Proteins - genetics; Fungal Proteins - metabolism; Fungi; Gene transfer; Gene Transfer, Horizontal; horizontal gene transfer; Ice; ice‐binding protein; Isoforms; Microorganisms; Nucleotide sequence; Phylogeny; protein structure; Proteins; Recrystallization; Sequence Homology, Amino Acid; Species Specificity
• ISSN: 1742-464X; 1742-4658
• DOI: 10.1111/febs.14725

Various microbes, including fungi and bacteria, that live in cold environments produce ice‐binding proteins (IBPs) that protect them from freezing. Ascomycota and Basidiomycota are two major phyla of fungi, and Antarctomyces psychrotrophicus is currently designated as the sole ascomycete that produces IBP (AnpIBP). However, its complete amino acid sequence, ice‐binding property, and evolutionary history have not yet been clarified. Here, we determined the peptide sequences of three new AnpIBP isoforms by total cDNA analysis and compared them with those of other microbial IBPs. The AnpIBP isoforms and ascomycete‐putative IBPs were found to be phylogenetically close to the bacterial ones but far from the basidiomycete ones, which is supported by the higher sequence identities to bacterial IBPs than basidiomycete IBPs, although ascomycetes are phylogenetically distant from bacteria. In addition, two of the isoforms of AnpIBP share low sequence identity and are not close in the phylogenetic tree. It is hence presumable that these two AnpIBP isoforms were independently acquired from different bacteria through horizontal gene transfer (HGT), which implies that ascomycetes and bacteria frequently exchange their IBP genes. The non‐colligative freezing‐point depression ability of AnpIBP was not very high, whereas it exhibited significant abilities of ice recrystallization inhibition, ice shaping, and cryo‐protection against freeze–thaw cycles even at submicromolar concentrations. These results suggest that HGT is crucial for the cold‐adaptive evolution of ascomycetes, and their IBPs offer freeze resistance to organisms to enable them to inhabit the icy environments of Antarctica. Databases Nucleotide sequence data are available in the DDBJ database under the accession numbers LC378707, LC378707, LC378707 for AnpIBP1a, AnpIBP1b, AnpIBP2, respectively. Ice‐binding proteins (IBPs) are cryoprotective polypeptides produced by various cold‐adapted microbes, such as bacteria and fungi. We identified two IBP genes from an Antarctic fungus, Antarctomyces psychrotrophicus. Phylogenetic analysis revealed that these two genes were possibly acquired from two different bacteria through horizontal gene transfer, which suggests that IBP genes are frequently exchanged between different microbes in Antarctica.