Peptidoglycan in obligate intracellular bacteria

Abstract

SummaryPeptidoglycan is the predominant stress‐bearing structure in the cell envelope of most bacteria, and also a potent stimulator of the eukaryotic immune system. Obligate intracellular bacteria replicate exclusively within the interior of living cells, an osmotically protected niche. Under these conditions peptidoglycan is not necessarily needed to maintain the integrity of the bacterial cell. Moreover, the presence of peptidoglycan puts bacteria at risk of detection and destruction by host peptidoglycan recognition factors and downstream effectors. This has resulted in a selective pressure and opportunity to reduce the levels of peptidoglycan. In this review we have analysed the occurrence of genes involved in peptidoglycan metabolism across the major obligate intracellular bacterial species. From this comparative analysis, we have identified a group of predicted ‘peptidoglycan‐intermediate’ organisms that includes the Chlamydiae, Orientia tsutsugamushi, Wolbachia and Anaplasma marginale. This grouping is likely to reflect biological differences in their infection cycle compared with peptidoglycan‐negative obligate intracellular bacteria such as Ehrlichia and Anaplasma phagocytophilum, as well as obligate intracellular bacteria with classical peptidoglycan such as Coxiella, Buchnera and members of the Rickettsia genus. The signature gene set of the peptidoglycan‐intermediate group reveals insights into minimal enzymatic requirements for building a peptidoglycan‐like sacculus and/or division septum.

Structure of the peptidoglycan polymerase RodA resolved by evolutionary coupling analysis

“…This mystery was resolved with the recent discovery that the highly conserved SEDS (shape, elongation, sporulation, and division) membrane proteins comprise a second class of peptidoglycan polymerases 1–3 (Figure 1a). In fact, SEDS proteins are even more widely distributed than aPBPs 1,7 . Despite their importance and broad phylogenetic distribution however, SEDS protein function is not well understood and no SEDS protein has been characterized structurally.…”

Dynamic expression of intra‐ and extra‐cellular proteome and the influence of epiphytic bacteria for Nostoc flagelliforme in response to rehydration

“…As shown in Fig. and Table S3, Murein DD‐endopeptidase MepM containing LysM domain, probable cytosol aminopeptidase and beta‐xylosidase were detected, while these enzymes were reported to participate in PG digestion (Otten et al ., ). The existence of LysM domains was widely reported for the resuscitation promoting factor (Rpf) proteins (Pinto et al ., ).…”

Building peptidoglycan inside eukaryotic cells: A view from symbiotic and pathogenic bacteria

“…Many cell division proteins, like the tubulin homologue FtsZ, are also missing in Chlamydiales with a division process that is orchestrated by the actin homologue MreB and its interactors RodZ and the LysM‐domain‐containing protein AmiA (NlpD), this latter with dual amidase and carboxypeptidase activities (Jacquier, Frandi, Viollier, & Greub, ; Jacquier, Viollier, et al, ; Klockner et al, , ). Such reduced number of periplasmic PG hydrolases is a hallmark of obligate intracellular pathogens (Otten et al, ) and endosymbionts (Wilmes et al, ), contrasting with the more than 35 PG hydrolases known in free‐living bacteria like E. coli (van Heijenoort, ; Vollmer, Joris, et al, ) (Figure b). Regarding proteins involved in PG biosynthesis, Chlamydiales have only two PBPs with TP domains that are homologs to E. coli PBP2 and PBP3(FtsI) and no enzyme known with canonical GT activity.…”

“…A vast number of biosynthetic and hydrolytic extracytosolic enzymes contribute to this PG structural plasticity. On an average, it is estimated that a minimum of 40 extracytosolic enzymes act on different bonds of the PG structure (Chodisetti & Reddy, 2019;Otten, Brilli, Vollmer, Viollier, & Salje, 2018;Sanders & Pavelka, 2013;Scheurwater, Reid, & Clarke, 2008;Vermassen et al, 2019). The bases for so many extracytosolic enzymes that exceed in number to what is needed to synthetize or cleave the bonds existing in the PG (Figure 1b), remain poorly understood.…”

“…Many cell division proteins, like the tubulin homologue FtsZ, are also missing in Chlamydiales with a division process that is orchestrated by the actin homologue MreB and its interactors RodZ and the LysM-domain-containing protein AmiA (NlpD), this latter with dual amidase and carboxypeptidase activities (Jacquier, Frandi, Viollier, & Greub, 2015;Klockner et al, 2018. Such reduced number of periplasmic PG hydrolases is a hallmark of obligate intracellular pathogens (Otten et al, 2018) and endosymbionts (Wilmes et al, 2017), contrasting with the more than 35 PG hydrolases known in free-living bacteria like E.…”