Systematic Survey for Novel Types of Prokaryotic Retroelements Based on Gene Neighborhood and Protein Architecture

• Published in: Molecular biology and evolution 2008-07, Vol.25 (7), p.1395-1404
• Main Authors: Kojima, Kenji K., Kanehisa, Minoru
• Format: Article
• Language: English
• Subjects: Amino Acid Sequence; Deoxyribonucleic acid; DNA; Eukaryotic Cells; Evolutionary biology; Genomics; Humans; Life cycles; Molecular biology; Molecular Sequence Data; Molecular structure; Nitrogen; Phylogeny; Prokaryotic Cells; Proteins; Proteins - chemistry; Proteins - genetics; Retroelements - genetics; RNA-Directed DNA Polymerase - genetics; Sequence Alignment
• ISSN: 0737-4038; 1537-1719
• DOI: 10.1093/molbev/msn081

Retroelements, elements encoding reverse transcriptase (RT), are ubiquitous in eukaryotes and have a great influence on the evolution of our genome. Detailed information is available on eukaryotic retroelements; however, prokaryotic retroelements are poorly understood. Recently, new types of eukaryotic retroelements were characterized on the basis of their gene composition and their phylogenetic positions. Here we performed a systematic survey to identify novel types of prokaryotic retroelements by analyzing gene neighborhood and protein architecture. We found novel types of gene combination and examined whether they represent actual retroelements. Five monophyletic groups were identified that were distinct from characterized prokaryotic retroelements, showed specific gene combination, were distributed patchily, and included at least 1 example of recent integration. These results strongly indicated the frequent horizontal transfer of these elements. One group encoded DNA polymerase A. A possible function of DNA polymerase A in the life cycle of retroelements is catalyzing second-strand cDNA synthesis, which is DNA polymerization performed using a DNA template not an RNA template. Another group encoded both bacterial primase and carbon-nitrogen hydrolase. Primase is likely to synthesize primers to initiate reverse transcription. Two other groups also encoded carbon-nitrogen hydrolase as a fusion protein with RT. It is difficult to speculate on the function of hydrolase in the life cycle of retroelements. The last group encoded dual RT proteins, which are likely to form heterodimers during replication. The protein sets of these 5 groups of prokaryotic retroelements were completely different from those of eukaryotic retroelements, indicating that the survival constraints of prokaryotic elements were distinct from those of eukaryotic elements. It is likely that these prokaryotic retroelements are maintained as extrachromosomal DNA or RNA or are accidentally integrated into genomes. Our findings presented the possibility that many types of extrachromosomal prokaryotic retroelements remain to be characterized. In addition, we found 8 RT genes were associated with clustered regularly interspaced short palindrome repeats (CRISPRs) of the CRISPR-Cas system. These RT genes are likely to work in immunity against RNA phages via cDNA synthesis.