Variation of the Virus-Related Elements within Syntenic Genomes of the Hyperthermophilic Archaeon Aeropyrum

Abstract

The increasing number of genome sequences of archaea and bacteria show their adaptation to different environmental conditions at the genomic level. Aeropyrum spp. are aerobic and hyperthermophilic archaea. Aeropyrum camini was isolated from a deep-sea hydrothermal vent, and Aeropyrum pernix was isolated from a coastal solfataric vent. To investigate the adaptation strategy in each habitat, we compared the genomes of the two species. Shared genome features were a small genome size, a high GC content, and a large portion of orthologous genes (86 to 88%). The genomes also showed high synteny. These shared features may have been derived from the small number of mobile genetic elements and the lack of a RecBCD system, a recombinational enzyme complex. In addition, the specialized physiology (aerobic and hyperthermophilic) of Aeropyrum spp. may also contribute to the entire-genome similarity. Despite having stable genomes, interference of synteny occurred with two proviruses, A. pernix spindle-shaped virus 1 (APSV1) and A. pernix ovoid virus 1 (APOV1), and clustered regularly interspaced short palindromic repeat (CRISPR) elements. Spacer sequences derived from the A. camini CRISPR showed significant matches with protospacers of the two proviruses infecting A. pernix, indicating that A. camini interacted with viruses closely related to APSV1 and APOV1. Furthermore, a significant fraction of the nonorthologous genes (41 to 45%) were proviral genes or ORFans probably originating from viruses. Although the genomes of A. camini and A. pernix were conserved, we observed nonsynteny that was attributed primarily to virus-related elements. Our findings indicated that the genomic diversification of Aeropyrum spp. is substantially caused by viruses. Between closely related organisms, gene repertoires and genome organizations differ depending on the ecological characteristics of each habitat. For example, whole-genomic comparisons of the cyanobacterial Prochlorococcus spp., with physiological features relevant to the different ecological niches within a stratified oceanic water column, show gross signatures of this niche differentiation (1). The members of the anaerobic hyperthermophilic archaeal genus Pyrococcus adapt to abiotic and biotic environmental conditions through positive gene selection (2). Although genomes of temperate coastal SAR11 isolates are highly conserved in the core genome common to all strains (3) and show synteny (the conservation of DNA sequence and gene order) (4), variations exist among genes for phosphorus metabolism, glycolysis, and C 1 metabolism. This suggests that adaptive specialization in nutrient resource utilization is important for niche partitioning (5).Aeropyrum species are heterotrophic, aerobic, neutrophilic, and hyperthermophilic archaea. The two currently known species, Aeropyrum pernix and Aeropyrum camini, were isolated from geographically distinct locations. The type strain of the type species, A. pernix K1, was isolated from a coastal solfataric vent on Kodakara-Jima Island in southwes...

Isolation and characterization of novel temperate virusAeropyrumglobular virus 1 infecting hyperthermophilic archaeonAeropyrum

“…ORF1_309). The GC content (55.8%) was similar to those of host chromosomes (50.7-56.7%) (25) and the reported dsDNA viruses infecting A. pernix (52.7-56.5%) (15, 23) ) but higher than those of other spherical viruses PSV (48%) (38) and TTSV (49.8%) (39). The AGV1 genome encoded 34 predicted ORFs starting from the ATG, GTG, and TTG codons (Table 3).…”

“…Further diversity in A. pernix viruses was predicted to have been still veiled in hot environments by transmission electron micrograph (TEM) observations (e.g., filamentous virus and short bacilliform virus) (23). Aeropyrum species are specialists in their habitat requirements and possess small and very conservative genomes (25). Genomic variation is observed in virus-related elements including two proviral regions (Fuselloviridae APSV1 and Guttaviridae APOV1), adaptive immune system against foreign genetic elements (clustered regularly interspaced short palindromic repeat [CRISPR]), and ORFans probably originating from viruses (25).…”

“…Aeropyrum species are specialists in their habitat requirements and possess small and very conservative genomes (25). Genomic variation is observed in virus-related elements including two proviral regions (Fuselloviridae APSV1 and Guttaviridae APOV1), adaptive immune system against foreign genetic elements (clustered regularly interspaced short palindromic repeat [CRISPR]), and ORFans probably originating from viruses (25). In addition, most spacer sequences (141/144) in the CRISPR loci of A. pernix K1 and A. camini SY1 showed no similarity to databases (25).…”

“…Genomic variation is observed in virus-related elements including two proviral regions (Fuselloviridae APSV1 and Guttaviridae APOV1), adaptive immune system against foreign genetic elements (clustered regularly interspaced short palindromic repeat [CRISPR]), and ORFans probably originating from viruses (25). In addition, most spacer sequences (141/144) in the CRISPR loci of A. pernix K1 and A. camini SY1 showed no similarity to databases (25). It is considered that their genomic diversification is mostly derived from viruses and that there are unknown viruses interacting with A. pernix and contribute to their population dynamics in the environment.…”

Genome variation in the hyperthermophilic archaeonAeropyrum

“…3,4 We recently determined the complete genome sequence of A. camini and compared it with the A. pernix genome 5 to determine the genetic differences between close relatives in distinct habitats. 6 The general genome features were similar between A. camini and A. pernix: small genome size (1.60 to 1.67 Mbp), G+C content (56.3 to 56.7%), and number of open reading frames (ORFs) (1645 to 1700). The genomic similarity score, which is calculated using the bit scores of shared orthologous genes, 7 was 0.87 and nucleotide identity between the two chromosomes was 73.2 to 76.6% over a wide range of the chromosomes (86.2 to 90.2%), indicating their close relationship.…”