Genome analysis and gene nblA identification of Microcystis aeruginosa myovirus (MaMV-DC) reveal the evidence for horizontal gene transfer events between cyanomyovirus and host

Abstract

The genome sequence, genetic characterization and nblA gene function of Microcystis aeruginosa myovirus isolated from Lake Dianchi in China (MaMV-DC) have been analysed. The genome DNA is 169 223 bp long, with 170 predicted protein-coding genes (001L-170L) and a tRNA gene. About one-sixth of these genes have homologues in the host cyanobacteria M. aeruginosa. The genome carries a gene homologous to host nblA, which encodes a protein involved in the degradation of cyanobacterial phycobilisome. Its expression during MaMV-DC infection was confirmed by reverse transcriptase PCR and Western blot detection and abundant expression was companied by the significant decline of phycocyanin content and massive release of progeny MaMV-DC. In addition, expressing MaMV-DC nblA reduced the phycocyanin peak and the phycocyanin to chlorophyll ratio in model cyanobacteria. These results confirm that horizontal gene transfer events have occurred between cyanobacterial host and cyanomyovirus and suggest that MaMV-DC carrying host-derived genes (such as 005L, that codes for NblA) is responsible for more efficient expression of cyanophage genes and release of progeny cyanophage. This study provides novel insight into the horizontal gene transfer in cyanophage and the interactions between cyanophage and their host.

Metabolic Genes within Cyanophage Genomes: Implications for Diversity and Evolution

“…Based on phylogenetic trees, these host-derived genes cluster with those from their potential host cyanobacteria, implying that they originated from cyanobacteria and supporting the evidence that cyanophages acquired these genes horizontally from their cyanobacterial hosts multiple times [58]. Additionally, in some genomes of freshwater cyanophages, an nblA gene was found to encode a small polypeptide present in all organisms containing phycobilisomes [34,35,38]. The cyanophage NblA has a high amino acid identity with its homologues in cyanobacteria.…”

“…A number of cultured cyanophage genomes have been completely sequenced [12,13,14,15,16,34,35,36,37,38,39,40,41,58,59], and revealed numerous DNA fragments of host-like metabolic gene origin, many of which encode important proteins for cellular and metabolic functions. There is increasing evidence that these host-like genes are frequently derived by phages through horizontal gene transfer from the viral gene pool or their hosts [39,60,61].…”

“…Through the deep sequencing of the phoH gene, the composition and diversity patterns of the phages in the Sargasso Sea were shown to be closely associated with spatio–temporal structure [109]. Also, phoH has been found in many cyanophages infecting cyanobacteria, such as marine cyanophages P-SSM2, P-SSM4 [41], Syn9 [15], and freshwater cyanophages Ma-LMM01 [34] and MaMV-DC [38]. From the analysis of the phoH phylogenetic tree, a high diversity of cyanophages has been found in all sampling sites [108].…”

“…They morphologically belong to three different double-stranded DNA virus families; Myoviridae , Podoviridae and Siphoviridae [30,31,32,33]. On the basis of the sequencing of complete genomes, it has been found that cyanophages contain unique genetic resources [12,13,14,15,16,34,35,36,37,38,39,40,41,42], a vast majority of which are considered as genome database orphans. Previously, it was suggested that these unique genes probably encode specific enzymes or proteins for the cyanophage life cycle [43,44].…”

A novel uncultured marine cyanophage lineage with lysogenic potential linked to a putative marine Synechococcus ‘relic’ prophage

“…Also, detected for the first time in marine cyanophages, genes coding for the phycobilisome degradation protein NblA were found in each of the newly identified cyanophages, and three of the MAGs contain two different copies of nblA . Single‐ nblA genes have been previously reported in freshwater cyanophages (Gao et al ., ; Ou et al ., ) that infect cyanobacteria using phycobilisomes for light harvesting. Phycobilisomes, large extrinsic multisubunit light‐harvesting complexes typical of most cyanobacteria, have been found in Synechococcus but not in Prochlorococcus (Dufresne et al ., ).…”