The nine peptidoglycan hydrolases genes in Lactobacillus helveticus are ubiquitous and early transcribed

Jebava, Iva; Plocková, M.; Lortal, Sylvie; Valence, Florence

doi:10.1016/j.ijfoodmicro.2011.04.015

Cited by 10 publications

(9 citation statements)

References 35 publications

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“…Notably, the closely related and S-layer-forming cheese-ripening bacterium L. helveticus DPC 4571 encodes 9 autolysins, including 5 orthologs from the PGH identified in this study (45). Redundancy of PGH within bacterial genomes is widespread (27) due to the essentiality of autolysin activity for cell survival (46).…”

Section: Discussionmentioning

confidence: 88%

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AcmB Is an S-Layer-Associated β- N -Acetylglucosaminidase and Functional Autolysin in Lactobacillus acidophilus NCFM

Johnson

Klaenhammer

2016

Appl Environ Microbiol

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Autolysins, also known as peptidoglycan hydrolases, are enzymes that hydrolyze specific bonds within bacterial cell wall peptidoglycan during cell division and daughter cell separation. Within the genome of Lactobacillus acidophilus NCFM, there are 11 genes encoding proteins with peptidoglycan hydrolase catalytic domains, 9 of which are predicted to be functional. Notably, 5 of the 9 putative autolysins in L. acidophilus NCFM are S-layer-associated proteins (SLAPs) noncovalently colocalized along with the surface (S)-layer at the cell surface. One of these SLAPs, AcmB, a β-N-acetylglucosaminidase encoded by the gene lba0176 (acmB), was selected for functional analysis. In silico analysis revealed that acmB orthologs are found exclusively in S-layer- forming species of Lactobacillus. Chromosomal deletion of acmB resulted in aberrant cell division, autolysis, and autoaggregation. Complementation of acmB in the ΔacmB mutant restored the wild-type phenotype, confirming the role of this SLAP in cell division. The absence of AcmB within the exoproteome had a pleiotropic effect on the extracellular proteins covalently and noncovalently bound to the peptidoglycan, which likely led to the observed decrease in the binding capacity of the ΔacmB strain for mucin and extracellular matrices fibronectin, laminin, and collagen in vitro. These data suggest a functional association between the S-layer and the multiple autolysins noncovalently colocalized at the cell surface of L. acidophilus NCFM and other S-layer-producing Lactobacillus species.IMPORTANCE Lactobacillus acidophilus is one of the most widely used probiotic microbes incorporated in many dairy foods and dietary supplements. This organism produces a surface (S)-layer, which is a self-assembling crystalline array found as the outermost layer of the cell wall. The S-layer, along with colocalized associated proteins, is an important mediator of probiotic activity through intestinal adhesion and modulation of the mucosal immune system. However, there is still a dearth of information regarding the basic cellular and evolutionary function of S-layers. Here, we demonstrate that multiple autolysins, responsible for breaking down the cell wall during cell division, are associated with the S-layer. Deletion of the gene encoding one of these S-layer-associated autolysins confirmed its autolytic role and resulted in reduced binding capacity to mucin and intestinal extracellular matrices. These data suggest a functional association between the S-layer and autolytic activity through the extracellular presentation of autolysins.

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Section: Discussionmentioning

confidence: 88%

“…It is also notable that there are two autolysins described in the PGH complement of L. helveticus DPC 4571 which contain the S-layer NCAD domain (45). …”

Section: Discussionmentioning

confidence: 99%

AcmB Is an S-Layer-Associated β- N -Acetylglucosaminidase and Functional Autolysin in Lactobacillus acidophilus NCFM

Johnson

Klaenhammer

2016

Appl Environ Microbiol

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“…Generally, a given bacterial species produces several PGHs that have various hydrolytic specificities, although not necessarily all the specificities listed above. In LAB, sequence analyses have revealed that rather complex PGH systems exist; 12 PGHs were identified in L. casei [21], 9 in L. helveticus [65], and 12 in L. plantarum [66]. Five PGHs were initially identified in L. lactis , before the description of the CHAP domain [67]; re-examination of the genome sequence of L. lactis MG1363 has allowed us to identify 4 additional putative PGHs that contain a CHAP domain (unpublished results).…”

Section: Peptidoglycanmentioning

confidence: 99%

Cell wall structure and function in lactic acid bacteria

2014

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The cell wall of Gram-positive bacteria is a complex assemblage of glycopolymers and proteins. It consists of a thick peptidoglycan sacculus that surrounds the cytoplasmic membrane and that is decorated with teichoic acids, polysaccharides, and proteins. It plays a major role in bacterial physiology since it maintains cell shape and integrity during growth and division; in addition, it acts as the interface between the bacterium and its environment. Lactic acid bacteria (LAB) are traditionally and widely used to ferment food, and they are also the subject of more and more research because of their potential health-related benefits. It is now recognized that understanding the composition, structure, and properties of LAB cell walls is a crucial part of developing technological and health applications using these bacteria. In this review, we examine the different components of the Gram-positive cell wall: peptidoglycan, teichoic acids, polysaccharides, and proteins. We present recent findings regarding the structure and function of these complex compounds, results that have emerged thanks to the tandem development of structural analysis and whole genome sequencing. Although general structures and biosynthesis pathways are conserved among Gram-positive bacteria, studies have revealed that LAB cell walls demonstrate unique properties; these studies have yielded some notable, fundamental, and novel findings. Given the potential of this research to contribute to future applied strategies, in our discussion of the role played by cell wall components in LAB physiology, we pay special attention to the mechanisms controlling bacterial autolysis, bacterial sensitivity to bacteriophages and the mechanisms underlying interactions between probiotic bacteria and their hosts.

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“…It can also result from the induction of a prophage in L. lactis and L. helveticus but this is not a general mechanism (Lortal and Chapot-Chartier 2005;Deutsch et al 2002Deutsch et al , 2003. In L. helveticus, which exhibits a large range of autolytic abilities (Valence et al 1998), the nine PGH genes are ubiquitous and transcribed early during growth in all the strains (Jebava et al 2011). The differences of autolytic properties of strains would result from differences in cell wall composition (Vinogradov et al 2013) (see Table 1 for further details).…”

Section: Formation Of Flavour Compounds By L Lactismentioning

confidence: 99%

Strain-to-strain differences within lactic and propionic acid bacteria species strongly impact the properties of cheese–A review

Thierry

Valence

Deutsch

et al. 2015

Dairy Sci. & Technol.

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Lactic acid bacteria (LAB) and propionic acid bacteria (PAB) are widely used in the manufacture of cheeses and other fermented dairy products. Bacterial species used as starters are mainly chosen according to their intrinsic properties: the milk acidifying capacity for LAB starters and the aromatizing properties of PAB, for example. Beyond the general characteristics of a bacterial species, many key phenotypic traits determining their interest for dairy applications depend on the strain within a given species. Through some examples, this review illustrates how the choice of a bacterial strain with specific technological characteristics, within a given species of LAB or PAB, can determine the final properties in the end product. This concerns the technological properties of cheeses, such as flavour, texture, and opening formation, and their functional properties, such as inhibition of undesirable microorganisms and health properties. When known, the genetic determinants of the diversity are presented. This review emphasizes the importance of preserving and exploring microbial resources at the intraspecific level, as an unending source of diversity for innovation in food fermentation.

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The nine peptidoglycan hydrolases genes in Lactobacillus helveticus are ubiquitous and early transcribed

Cited by 10 publications

References 35 publications

AcmB Is an S-Layer-Associated β- N -Acetylglucosaminidase and Functional Autolysin in Lactobacillus acidophilus NCFM

AcmB Is an S-Layer-Associated β- N -Acetylglucosaminidase and Functional Autolysin in Lactobacillus acidophilus NCFM

Cell wall structure and function in lactic acid bacteria

Strain-to-strain differences within lactic and propionic acid bacteria species strongly impact the properties of cheese–A review

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