Reductive evolution and unique infection and feeding mode in the CPR predatory bacteriumVampirococcus lugosii

Abstract

The Candidate Phyla Radiation (CPR) constitutes a large supergroup of mostly uncultured bacterial lineages discovered through metabarcoding and metagenomics in diverse environments. Having small cell sizes, reduced genomes, and limited biosynthetic capabilities, they are thought to be symbionts of other organisms from which they obtain essential biomolecules. However, the nature of this symbiosis (mutualistic, neutral, or parasitic) has been ascertained only for rare cultured members of the CPR phylum Saccharibacteria, which are epibiotic parasites of other bacteria. Here, we characterize the biology and the genome of Vampirococcus lugosii, which becomes the first described species of Vampirococcus, a genus of epibiotic bacteria morphologically identified decades ago. Vampirococcus belongs to the CPR phylum Absconditabacteria. It feeds on anoxygenic photosynthetic gammaproteobacteria, fully absorbing their cytoplasmic content. The cells divide epibiotically, forming multicellular stalks whose apical cells can more easily reach new hosts. Vampirococcus genome is small (1.3 Mbp) and highly reduced in biosynthetic metabolism genes. However, it is enriched in genes related to an elaborate, fibrous cell surface likely involved in complex interactions with the host. Comparative genomic analyses show that gene loss has been continuous during Absconditabacteria, and generally most CPR bacteria, evolution. Nonetheless, gene loss was compensated by gene acquisition by horizontal gene transfer and evolution de novo. In Vampirococcus, these innovations include new CRISPR-Cas effectors and a novel electron transport chain. Our findings confirm parasitism as a widespread lifestyle of CPR bacteria, which probably play a previously neglected virus-like ecological role in ecosystems, controlling bacterial populations by a unique form of predation.

Physical connections: prokaryotes parasitizing their kin

“…D. TEM picture of the SR1 phylum (CPR) member Vampirococcus lugosii parasitizing its anoxygenic photosynthetic bacterial host Halochromatium sp. (Moreira et al ., 2020). The bar size corresponds to 500 nm.…”

“…2). Another clear example of parasitic interaction is that of Vampirococcus lugosii , a member of the CPR phylum Absconditabacteria, which preys on anoxygenic photosynthetic gammaproteobacteria of the genus Halochromatium , consuming its cytoplasmic content and killing it (Moreira et al ., 2020). This is indeed the first described species of Vampirococcus , a genus of predatory bacteria first portrayed by optical and electron microscopy observations more than 20 years ago (Guerrero et al ., 1986).…”

“…The peculiar nature of CPR cell surface may be related to host recognition and infectivity (Luef et al, 2015). It is known that TM7x displays a (Moreira et al, 2020). The bar size corresponds to 500 nm.…”

Patterns of gene content and co-occurrence constrain the evolutionary path toward animal association in CPR bacteria

“…Compared to Saccharibacteria, host relationships for Gracilibacteria and Absconditabacteria have received little attention. There are preliminary indications that Absconditabacteria may associate with members of the Fusobacteria or Firmicutes in the oral microbiome (44) or the gammaproteobacterium Halochromatium in certain salt lakes (84). We thus explored co-occurrence patterns in microbial communities containing Absconditabacteria and Gracilibacteria, attempting to further constrain possible host taxa.…”

Metagenome-derived virus-microbe ratios across ecosystems

“…The few described DPANN and CPR members correspond to small obligate symbiotic cells physically attached to prokaryotic hosts. Some of them, notably CPR bacteria, are parasites/predators 26,27 ; others can display mutualistic interactions (e.g. complementation of host’s metabolism to degrade specific substrates 28 ) although, upon environmental change, they likely behave as parasites, shifting along the mutualism-parasitism continuum 29 .…”