A novel virus lineage is abundant in metaviromes from Dehalococcoides-containing mixed cultures

Abstract

Dehalococcoides mccartyi are obligately anaerobic organohalide-respiring bacteria that play important roles in the detoxification of chlorinated pollutants in groundwater and sediments. Despite having small genomes, they host a diverse set of mobile elements. Here we characterize a family of mobile elements, termed integrative and mobilizable element 1 or IME1, comprising 20 from Dehalococcoides and one from Dehalogenimonas alkenigignens. IME1s are 20,930 – 28,058 bp and are found both integrated in the genomes and as circular episomes. Bioinformatic characterization of IME1 encoded proteins revealed a highly conserved structure with 14 hierarchical orthologous groups (HOGs) found in all 21 IME1s. IME1s lack recognizable hallmark proteins of tailed bacterial viruses (or tailed phages) but encode proteins with similarities to those of filamentous bacterial viruses. In particular, one conserved HOG shows sequence similarity to the pI-like ATPase, the only conserved marker protein identified across filamentous bacterial viruses. Additionally, IME1s encode several small proteins with predicted transmembrane domains and signal peptides, another feature used to identify filamentous bacterial viruses. Both features are also found in budding archaeal viruses of various morphotypes. IME1s dominated metaviromes obtained from the Dehalococcoides-containing KB-1 mixed culture and electron micrographs of the corresponding viral fractions revealed abundant filamentous virus-like particles. We therefore propose that the IME1s represent a novel lineage of double stranded budding, likely filamentous, viruses. Database searches suggest IME1s are found in Dehalococcodia and other Chlorofexota but are so far restricted to this phylum. Importance Dehalococcoides are obligate organohalide respiring anaerobic bacteria that use halogenated organic compounds as terminal electron acceptors and are important for bioremediation of polluted sites. Here we describe IME1s, a novel group of viruses associated with Dehalococcoidia that we propose have double stranded DNA (dsDNA) genomes and a non-lytic, likely filamentous lifestyle. IME1s share features with both characterized filamentous bacterial viruses, which package small single stranded DNA (ssDNA) genomes, and archaeal budding viruses, often with larger dsDNA genomes. IME1s expand the known diversity of bacterial viruses and may help reveal how viruses influence the bacteria that detoxify contaminated sites.