Abstract
Deep-sea hydrothermal vent environments are characterized by high hydrostatic pressure and sharp temperature and chemical gradients. Horizontal gene transfer is thought to play an important role in the microbial adaptation to such an extreme environment. In this study, a 21.4-kb DNA fragment was identified as a genomic island, designated PYG1, in the genomic sequence of the piezophilic hyperthermophile Pyrococcus yayanosii. According to the sequence alignment and functional annotation, the genes in PYG1 could tentatively be divided into five modules, with functions related to mobility, DNA repair, metabolic processes and the toxin-antitoxin system. Integrase can mediate the site-specific integration and excision of PYG1 in the chromosome of P. yayanosii A1. Gene replacement of PYG1 with a SimR cassette was successful. The growth of the mutant strain ΔPYG1 was compared with its parent strain P. yayanosii A2 under various stress conditions, including different pH, salinity, temperature, and hydrostatic pressure. The ΔPYG1 mutant strain showed reduced growth when grown at 100°C, while the biomass of ΔPYG1 increased significantly when cultured at 80 MPa. Differential expression of the genes in module III of PYG1 was observed under different temperature and pressure conditions. This study demonstrates the first example of an archaeal integrative genomic island that could affect the adaptation of the hyperthermophilic piezophile P. yayanosii to high temperature and high hydrostatic pressure.
Highlights
Deep-sea hydrothermal vent environments are characterized by high hydrostatic pressure (HHP) and sharp temperature and chemical gradients (Reysenbach et al, 2006; Oger and Jebbar, 2010)
The transcriptome of the piezophile Photobacterium profundum SS9 grown under different pressure (28 MPa vs. 45 MPa) and temperature (4◦C vs 16◦C) conditions was analyzed, and the results showed that there were differentially expressed genes that belonged to three genomic islands (GIs) (Chr1.8, Chr2.3, and Chr2.5) in the SS9 genome; these genes are absent in both the pressure-sensitive strain 3TCK and the pressure-adapted strain DSJ4 (Campanaro et al, 2005)
We characterized the largest GI PYG1 in P. yayanosii, which showed high sequence similarity to its counterparts within T. barophilus MP as either a GI TBG1 in the chromosome or a DNA fragment in plasmid pTBMP1 (Marteinsson et al, 1999; Vannier et al, 2011). Both ends of the GIs PYG1 and TBG1 were aligned as functional modules, reflecting a GI frame that is capable of site-specific integration
Summary
Deep-sea hydrothermal vent environments are characterized by high hydrostatic pressure (HHP) and sharp temperature and chemical gradients (Reysenbach et al, 2006; Oger and Jebbar, 2010). The microorganisms dwelling here are expected to show strong high temperature adaptation (Jebbar et al, 2015). Mobile genetic elements, such as plasmids, bacteriophages, transposons, Genomic Island Affects Pyrococcus Adaptation integrons, conjugative transposons, integrative conjugative elements (ICEs), and genomic islands (GIs), are important and essential components of the marine biosphere that promote marine microbial diversification (Sobecky and Hazen, 2009). Many of the accessory genes acquired by HGT form syntenic blocks recognized as GIs (Juhas et al, 2009). These gene fragments are often inserted into tRNA gene loci, which act as integration sites for foreign DNA, mainly prophages, and are flanked by direct repeats (DRs) that consist of a few to more than a hundred nucleotides. Integrases, transposases, ISs, and other mobility genes encoded in GIs can be involved in the integration, mobility, deletion, and rearrangement of GIs (Darmon and Leach, 2014)
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