Novel chaperonins are prevalent in the virioplankton and demonstrate links to viral biology and ecology

Abstract

Chaperonins are protein-folding machinery found in all cellular life. Chaperonin genes have been documented within a few viruses, yet, surprisingly, analysis of metagenome sequence data indicated that chaperonin-carrying viruses are common and geographically widespread in marine ecosystems. Also unexpected was the discovery of viral chaperonin sequences related to thermosome proteins of archaea, indicating the presence of virioplankton populations infecting marine archaeal hosts. Virioplankton large subunit chaperonin sequences (GroELs) were divergent from bacterial sequences, indicating that viruses have carried this gene over long evolutionary time. Analysis of viral metagenome contigs indicated that: the order of large and small subunit genes was linked to the phylogeny of GroEL; both lytic and temperate phages may carry group I chaperonin genes; and viruses carrying a GroEL gene likely have large double-stranded DNA (dsDNA) genomes (>70 kb). Given these connections, it is likely that chaperonins are critical to the biology and ecology of virioplankton populations that carry these genes. Moreover, these discoveries raise the intriguing possibility that viral chaperonins may more broadly alter the structure and function of viral and cellular proteins in infected host cells.

Single-cell genomics uncover Pelagibacter as the putative host of the extremely abundant uncultured 37-F6 viral population in the ocean

“…"gene signatures") encoding the above mentioned capsid protein (Fig. 2c), previously characterized to be the most abundant in marine viral proteomes [19], a terminase (TerL), and a chaperonin Gro-Es, recently described to be widespread in marine virosphere and always placed upstream from capsid genes [25], as found in this case. Furthermore, the uncultured pelagiphages in SAG AG-470-G06 and AG-422-I02 had a gene annotated as "genome maintenance exonuclease 1" at JGI-IMG, that was also present in the bacterial genome of 18 different Pelagibacter SAGs ( Supplementary Table 8), including SAG MED40; all of them from oligotrophic environments.…”

Xanthomonas citri jumbo phage XacN1 exhibits a wide host range and high complement of tRNA genes

“…During phage replication, chaperonin is usually supplied from the host and involved in the generation of phage particles 35 . However, recent metagenomic data indicated that chaperonin-encoding viruses are more common than previously thought and geographically widespread in marine ecosystems 36 , 37 . By encoding its own chaperonin, XacN1 virion assembly process might not be totally dependent on the host chaperonin machinery.…”

Structure and conformational cycle of a bacteriophage-encoded chaperonin

“…each subunit in one ring interacts with two subunits in the opposing ring, whereas the subunits in group II chaperonins interact in a one to one fashion. 7 of ɸEL and GroEL ( 0.2 µM tetradecamer) in the absence or presence of GroES (0.4 µM heptamer) or 0.8 µM denatured DM-MBP (diluted from 6M GuHCl, final ~20 mM) were performed in LS or HS buffer and in presence of 1 mM ATP. The ATPase activity of ɸEL (0.2 µM tetradecamer) was also measured with increasing concentrations of GroES.…”

“…Thus, ɸEL may represent an evolutionary more ancient chaperonin prior to acquisition of the encapsulation mechanism.4 Evolutionary more distant chaperonin homologs were discovered in the genomes of bacteriophages. While many phages encode only a GroES homolog that cooperates with the host GroEL [6], some have both GroEL and GroES homologs and few encode only a GroEL-like chaperonin [7]. The latter group includes the protein gp146 from the bacteriophage EL of Pseudomonas aeruginosa [8,9], henceforth referred to as ɸEL.…”