Genomic evidence for inter-class host transition between abundant streamlined heterotrophs by a novel and ubiquitous marine Methylophage

Abstract

The methylotrophic OM43 clade are Gammaproteobacteria that comprise some of the smallest free-living cells known with highly streamlined genomes. OM43 represents an important microbial link between marine primary production and return of carbon back to the atmosphere. Bacteriophages shape microbial communities and are major drivers of mortality and global marine biogeochemistry. Recent cultivation efforts have brought the first viruses infecting members of the OM43 clade into culture. Here we characterize a novel myophage infecting OM43, called Melnitz. Melnitz was isolated independently on three separate occasions (with isolates sharing >99.95% average nucleotide identity) from water samples from a subtropical ocean gyre (Sargasso Sea) and temperate coastal (Western English Channel) systems. Metagenomic recruitment from global ocean viromes confirmed that Melnitz is globally ubiquitous, congruent with patterns of host abundance. Bacteria with streamlined genomes such as OM43 and the globally dominant SAR11 clade use riboswitches as an efficient method to regulate metabolism. Melnitz encodes a two-piece tmRNA (ssrA), controlled by a glutamine riboswitch, providing evidence that riboswitch use also occurs for regulation during phage infection of streamlined heterotrophs. Virally encoded tRNAs and ssrA found in Melnitz were phylogenetically more closely related to those found within the alphaproteobacterial SAR11 clade and their associated myophages than those within their gammaproteobacterial hosts. This suggests the possibility of an ancestral inter-class host transition event between SAR11 and OM43. Melnitz and a related myophage that infects SAR11 were unable to infect hosts of the SAR11 and OM43, respectively, suggesting host transition rather than a broadening of host range.

Long-read powered viral metagenomics in the Oligotrophic Sargasso Sea

“…To date, our understanding of the structure of the viral communities in the Sargasso Sea have been limited to seasonal patterns in abundances of viral-like particles (Parsons et al, 2012) and genomic analysis of isolated phages (Sullivan et al, 2005(Sullivan et al, , 2010Kelly et al, 2013;Zhao et al, 2013;Buchholz et al, 2021a). Here, we used metagenomics to characterise the viral communities at 80m and 200m in both the cellular and viral fractions of the stratified Sargasso Sea during a four-day cruise in July 2017.…”