Molecular Basis for the Maintenance of Envelope Integrity in Selenomonas ruminantium: Cadaverine Biosynthesis and Covalent Modification into the Peptidoglycan Play a Major Role

Abstract

Summary Polyamine is a small organic polycation composed of a hydrocarbon backbone with multiple amino groups which ubiquitously exists in all living organisms from bacteria to higher animals. The critical step of polyamine biosynthesis generally includes the amino acid-decarboxylating reaction to produce the primary diamines, such as a synthesis of putrescine (NH 3 ϩ ·(CH 2 ) 4 ·NH 3 ϩ ) from ornithine, and cadaverine (NH 3 ϩ ·(CH 2 ) 5 ·NH 3 ϩ ) from lysine, which are catalyzed by pyridoxal-5 ′ -phosphate (PLP; vitamin B 6 )-dependent decarboxylases. Synthesized polyamines are implicated in a wide variety of cytoplasmic reactions such as DNA replication and protein synthesis, and are essential for proper growth of the organisms. However, in Selenomonas ruminantium , a strictly anaerobic Gram-negative bacterium dominant in sheep rumen, cadaverine displays its function in a quite distinctive scheme compared to the general bacteria reported. It serves as an essential constituent of the peptidoglycan for the maintenance of envelope integrity through an interaction with the periplasm-exposed SLH domain of Mep45, the outer membrane protein of this bacterium. Furthermore, cytoplasmic biosynthesis of cadaverine occurs totally in a eukaryotic-like manner rather than in a conventional way of bacteria. Lysine/ornithine decarboxylase (LDC/ODC), a PLP-dependent enzyme responsible for cadaverine synthesis in this bacterium, displays significant homology to the eukaryotic ODC but not to the general bacterial LDC nor ODC, and its activity is tightly regulated by antizyme-mediated proteolysis, a regulatory process generally found in eukaryotes. These findings represent the biological diversity of this bacterium beyond the preexisting knowledge related to the polyamine-physiology, cell envelope-architecture, and the regulatory system for the enzyme. In this review we will describe (i) the cadaverine-containing peptidoglycan of S. ruminantium : its chemical structure, biosynthesis, and biological function, and (ii) cellular biosynthesis of cadaverine by LDC/ODC and its antizyme-mediated regulation. In addition, we will briefly refer to (iii) the phylogenetic position and characteristics of S. ruminantium and its unique cadaverine-physiology.

Outer Membrane Proteome of Veillonella parvula: A Diderm Firmicute of the Human Microbiome

“…This correlates well with the function as an OM tether, as in E. coli Braun's lipoprotein is the most numerous protein in the cell (Braun, 1975). Furthermore, this supports the hypothesis that all Negativicutes utilize OmpM as a form of attachment (Kojima and Kamio, 2012). Moreover, this is consistent with a transcriptomics study of three Veillonella species from the mouth, which found all three copies of OmpM to be the most abundant OM transcripts (Do et al, 2015), further highlighting the importance of these proteins (Kojima et al, 2016).…”

“…OmpM is an alternative method for tethering the OM to the peptidoglycan by binding of polyamine-modified peptidoglycan through an S-Layer homology (SLH) domain and a transmembrane β-barrel for OM attachment (Kojima and Kamio, 2012). This contrasts with Escherichia coli's Braun's lipoprotein (Lpp), which covalently binds PG and integrates into the OM via a lipid moiety (Braun and Rehn, 1969).…”

Bacterial outer membrane constriction

“…Selenomonas , another genus of the Negativicutes, appears to be the only genus of Gram‐negatives with no OmpA‐like domain‐containing proteins or Lpp. Selenomonas do, however, have a peptidoglycan modified with the polyamine cadaverine which is bound by an alternative OMP, OmpM (Mep45) by virtue of a SLH (S‐layer homologous) domain (Kojima et al ., ), this connection is important for OM integrity (Kojima et al ., ; Kojima and Kamio, ). No information on OM constriction during cell division in the Negativicutes is currently available.…”

One or two membranes? Diderm Firmicutes challenge the Gram‐positive/Gram‐negative divide

“…Another feature of the diderm Firmicutes envelope that has been studied is the mechanism of OM attachment, completely different from that of E. coli (Kojima et al, 2010). E. coli utilizes Braun's lipoprotein (Lpp) (Braun & Rehn, 1969) and other redundant systems such as Pal (Cascales et al, 2002) and OmpA (Park et al, 2011) for attachment of the OM, whereas Selenomonas ruminantium was shown to bind polyamine-modified peptidoglycan to the OM through a protein that contains an S-Layer homology domain (SLH) and a porin domain (OmpM) (Kojima & Kamio, 2012).…”