Abstract

Members of the major candidate phylum Dependentiae (a.k.a. TM6) are widespread across diverse environments from showerheads to peat bogs; yet, with the exception of two isolates infecting amoebae, they are only known from metagenomic data. The limited knowledge of their biology indicates that they have a long evolutionary history of parasitism. Here, we present Chromulinavorax destructans (Strain SeV1) the first isolate of this phylum to infect a representative from a widespread and ecologically significant group of heterotrophic flagellates, the microzooplankter Spumella elongata (Strain CCAP 955/1). Chromulinavorax destructans has a reduced 1.2 Mb genome that is so specialized for infection that it shows no evidence of complete metabolic pathways, but encodes an extensive transporter system for importing nutrients and energy in the form of ATP from the host. Its replication causes extensive reorganization and expansion of the mitochondrion, effectively surrounding the pathogen, consistent with its dependency on the host for energy. Nearly half (44%) of the inferred proteins contain signal sequences for secretion, including many without recognizable similarity to proteins of known function, as well as 98 copies of proteins with an ankyrin-repeat domain; ankyrin-repeats are known effectors of host modulation, suggesting the presence of an extensive host-manipulation apparatus. These observations help to cement members of this phylum as widespread and diverse parasites infecting a broad range of eukaryotic microbes.

Highlights

  • The candidate phylum Dependentiae is a phylogenetic group of bacteria that is only known from metagenomic data and from two isolates that infect free-living amoebae

  • Little is known about the biology of bacteria in the candidate phylum Dependentiae, despite being widespread in nature

  • We describe a novel isolate of this phylum, Chromulinavorax destructans, which infects an abundant aquatic predatory protist, Spumella

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Summary

Introduction

The candidate phylum Dependentiae ( known as TM6) is a phylogenetic group of bacteria that is only known from metagenomic data and from two isolates that infect free-living amoebae. Relatively little is known about members of the Dependentiae, analysis of environmental 16S-ribosomal RNA sequences and metagenomic data indicate that they are widespread across diverse environments including peat bogs [1], hospital biofilms, soil, and waste water [2, 3] Analysis of these data imply that bacteria in this phylum have very limited metabolic capability, but encode an extensive system of transporters, including ATP transporters, as well as genes functions enriched in bacterial endosymbionts such as Chlamydia, Wolbachia, and Rickettsia, suggesting that bacteria in the Dependentiae are symbionts or parasites that rely extensively on eukaryotic hosts for energy and metabolites [2, 3]. Since the genome of Babela massiliensis is the only complete genome available for the members of the Dependentiae, a detailed comparison of the genomic complement involved in the different lifestyles is not possible; yet, several almost-complete metagenomically assembled genomes (MAGs) for other members of the phylum suggest that they are distinct from those infecting amoebae [6,7,8]

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