The candidate phylum Poribacteria by single-cell genomics: new insights into phylogeny, cell-compartmentation, eukaryote-like repeat proteins, and other genomic features

Abstract

The candidate phylum Poribacteria is one of the most dominant and widespread members of the microbial communities residing within marine sponges. Cell compartmentalization had been postulated along with their discovery about a decade ago and their phylogenetic association to the Planctomycetes, Verrucomicrobia, Chlamydiae superphylum was proposed soon thereafter. In the present study we revised these features based on genomic data obtained from six poribacterial single cells. We propose that Poribacteria form a distinct monophyletic phylum contiguous to the PVC superphylum together with other candidate phyla. Our genomic analyses supported the possibility of cell compartmentalization in form of bacterial microcompartments. Further analyses of eukaryote-like protein domains stressed the importance of such proteins with features including tetratricopeptide repeats, leucin rich repeats as well as low density lipoproteins receptor repeats, the latter of which are reported here for the first time from a sponge symbiont. Finally, examining the most abundant protein domain family on poribacterial genomes revealed diverse phyH family proteins, some of which may be related to dissolved organic posphorus uptake.

Figure 1. Phylogenomic tree based on a concatenated alignment of up to 83 genes illustrating the phylogenetic position of the candidate phylum Poribacteria.

Bootstrap value (100 resamplings) are shown on tree nodes where support ≥50%. Number of genomes per group is displayed in group boxes. Outgroup consists of several species of Spirochaetes and Gammaproteobacteria. The scale bar represents 10% sequence divergence.

Figure 2. 16S rRNA gene based maximum likelihood tree illustrating the phylogenetic position of the candidate phylum Poribacteria.

Bootstrap values (500 resamplings) ≥50% are shown on tree nodes. Numbers of sequences included per group is shown in group boxes. Outgroup consists of 80 sequences belonging to the Bacteroidetes. Scale bar represents 10% sequences divergence.

Figure 3. Schematic view of poribacterial BMC shell protein groups.

For a better overview all genes are displayed in 5′-3′ direction of the BMC shell protein gene. The actual strand orientation might be different and is indicated by plus or minus signs. Genes are shown with locus taq and amino acid identities based on IMG/MER homology searches are shown between genes where applicable. BMC shell protein genes are shown in white, other genes with homologies between different SAGs are shown in dark grey, other genes are shown in light grey.

Figure 4. Bar plot showing frequency of eukaryote-like pfam domains found on poribacterial SAGs in comparison to the average and maximum frequency on all finished genomes of marine free-living bacteria available in IMG in July 2013.