Comparative Genomics of Four Isosphaeraceae Planctomycetes: A Common Pool of Plasmids and Glycoside Hydrolase Genes Shared by Paludisphaera borealis PX4T, Isosphaera pallida IS1BT, Singulisphaera acidiphila DSM 18658T, and Strain SH-PL62

Abstract

The family Isosphaeraceae accommodates stalk-free planctomycetes with spherical cells, which can be assembled in short chains, long filaments, or aggregates. These bacteria inhabit a wide variety of terrestrial environments, among those the recently described Paludisphaera borealis PX4T that was isolated from acidic boreal wetlands. Here, we analyzed its finished genome in comparison to those of three other members of the Isosphaeraceae: Isosphaera pallida IS1BT, Singulisphaera acidiphila DSM 18658T, and the uncharacterized planctomycete strain SH-PL62. The complete genome of P. borealis PX4T consists of a 7.5 Mb chromosome and two plasmids, 112 and 43 kb in size. Annotation of the genome sequence revealed 5802 potential protein-coding genes of which 2775 could be functionally assigned. The genes encoding metabolic pathways common for chemo-organotrophic bacteria, such as glycolysis, citrate cycle, pentose-phosphate pathway, and oxidative phosphorylation were identified. Several genes involved in the synthesis of peptidoglycan as well as N-methylated ornithine lipids were present in the genome of P. borealis PX4T. A total of 26 giant genes with a size >5 kb were detected. The genome encodes a wide repertoire of carbohydrate-active enzymes (CAZymes) including 44 glycoside hydrolases (GH) and 83 glycosyltransferases (GT) affiliated with 21 and 13 CAZy families, respectively. The most-represented families are GH5, GH13, GH57, GT2, GT4, and GT83. The experimentally determined carbohydrate utilization pattern agrees well with the genome-predicted capabilities. The CAZyme repertoire in P. borealis PX4T is highly similar to that in the uncharacterized planctomycete SH-PL62 and S. acidiphila DSM 18658T, but different to that in the thermophile I. pallida IS1BT. The latter strain has a strongly reduced CAZyme content. In P. borealis PX4T, many of its CAZyme genes are organized in clusters. Contrary to most other members of the order Planctomycetales, all four analyzed Isosphaeraceae planctomycetes have plasmids in numbers varying from one to four. The plasmids from P. borealis PX4T display synteny to plasmids from other family members, providing evidence for their common evolutionary origin.

Anticancer Activity in Planctomycetes

“…However, Planctomycetes have recently been recognized as important producers of bioactive compounds by both in silico genome mining analyses and molecular screening approaches. These analyses revealed the presence of genes related to various pathways for the production of several bioactive molecules, including some antitumor compounds like epothilone (Donadio et al, 2007;Graça et al, 2013;Wang et al, 2014;Graça et al, 2016;Ivanova et al, 2017;Vollmers et al, 2017). It is therefore very promising that several of our Planctomycetes strains isolated from various ecosystems showed significant cytotoxic activity toward the MOLM-13 cells and the human prostatic PC3 cells.…”

Genome Analysis of Fimbriiglobus ruber SP5T, a Planctomycete with Confirmed Chitinolytic Capability

“…Recently, the gene encoding the key enzyme for synthesis of N-methylated phosphorus-free ornithine membrane lipids, N-methyltransferase (OlsG), was identified in the genome of Singulisphaera acidiphila DSM 18658 T (Sinac_1600) (24) and later detected in genomes of other members of the family Isosphaeraceae (11). Our analysis revealed that distant homologs of Sinac_1600 are also present in the genomes of Gemmataceae planctomycetes, including F. ruber SP5 T , Zavarzinella formosa A10 T , and Gemmata sp.…”

“…Members of the family Isosphaeraceae are especially abundant in boreal peatlands (9,10). As revealed by recent comparative genomic analysis, these peat-inhabiting planctomycetes possess extremely high but partly hidden glycolytic potential (11) and are capable of degrading various heteropolysaccharides. The ability to degrade fibrous and microcrystalline cellulose, however, has so far been demonstrated only for a single, peat-inhabiting planctomycete from the family Gemmataceae, Telmatocola sphagniphila (12).…”

Dynamics of active potential bacterial and fungal interactions in the assimilation of acidobacterial EPS in soil

“…Members of the order Phycisphaerales and genus Zavarzinella also responded to xylan, while group WD2101 were responsive to cellulose and chitin. Another study by Ivanova et al (2017b) further supported the high glycolytic potential of Planctomycetes. In that study, a comparative genomic analysis of 4 members of the family Isosphaeraceae, namely Isosphaera pallida, Singulisphaera acidiphila, Paludisphaera borealis and the uncharacterized strain SH-PL62S, identified several CAZYmes from major families (GH5, GH13, GH57) as well as potential α-mannosidase, α-rhamnosidase and glucuronyl hydrolase activities.…”

“…The most abundant bacterial genus in the "heavy" fraction, Singulisphaera, had mostly positive connections, especially with other groups of Planctomycetes, Actinobacteria and Verrucomicrobia, suggesting potential cooperation for metabolizing WH15EPS. Several studies demonstrate that those groups of bacteria have glycolytic and detoxifying capacities, producing several enzymes that could be involved in the degradation of the EPS and resource sharing (Martinez-Garcia et al, 2012;Uhlik et al, 2012;Ivanova et al, 2017b). In addition, no direct correlation was found between Singulisphaera and the EPS producer Granulicella, which suggests that the metabolism of WH15EPS by Singulisphaera and enrichment of the genus did not negatively impact the abundance of Granulicella.…”