Cell wall structure and function in lactic acid bacteria

Chapot-Chartier and Kulakauskas Microbial Cell Factories 2014, 13(Suppl 1):S9 http://www.microbialcellfactories.com/content/13/S1/S9 PROCEEDINGS Open Access Cell wall structure and function in lactic acid bacteria Marie-Pierre Chapot-Chartier1,2*, Saulius Kulakauskas1,2 From 11th International Symposium on Lactic Acid Bacteria Egmond aan Zee, the Netherlands. 31 August - 4 September 2014 Abstract 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 Grampositive 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. Introduction The cell wall of Gram-positive bacteria is a complex arrangement of macromolecules. It consists of a peptidoglycan (PG) sacculus that surrounds the cytoplasmic membrane and that is decorated with other glycopolymers, such as teichoic acids (TAs) or polysaccharides (PSs), and proteins. The cell wall has multiple functions during bacterial growth, including maintaining bacterial cell integrity and shape as well as resisting internal turgor pressure. Furthermore, it must remain flexible to accommodate the remodeling that is required for cell division and growth. Since it serves as the interface between the bacterial cell and its environment, the cell wall also mediates bacterial interactions with abiotic surfaces, infecting bacteriophages, or eukaryotic host cells. * Correspondence: 1 INRA, UMR1319 Micalis, F-78350 Jouy-en-Josas, France Full list of author information is available at the end of the article Lactic acid bacteria (LAB) are Gram-positive bacteria that belong to numerous genera, including Lactococcus, Enterococcus, Oenococcus, Pediococcus, Streptococcus, and Lactobacillus [1-3]. These bacteria metabolize sugars, mainly converting them to lactic acid, and are widely used as starters in the fermentation of food such as meat, vegetables, fruit, beverages, and milk. They play key roles in food preservation and contribute to the development of food texture and flavor [4,5]. Furthermore, LAB are present in the human gut microbiota. Certain natural LAB strains, lactobacilli strains in particular, are commercially sold as probiotics with health-promoting properties [6]. Finally, due to their GRAS (generally recognized as safe) status, LAB may be suitable vectors for the delivery of therapeutic proteins or antigens to mucosal surfaces [7,8]. When it comes to the technological and health applications of LAB, cell wall composition, structure, and © 2014 Chapot-Chartier and Kulakauskas; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Chapot-Chartier and Kulakauskas Microbial Cell Factories 2014, 13(Suppl 1):S9 http://www.microbialcellfactories.com/content/13/S1/S9 component organization play major roles. The LAB cell wall has been the subject of research because it contains receptors for bacteriophages that threaten milk fermentation [9,10]. Research has also focused on the need to favor LAB cell wall disruption to provoke autolysis, so that, during cheese ripening, bacteria release their cytoplasmic content, which is rich in enzymes involved in the development of organoleptic properties [11]. It has also been suggested that increasing bacterial lysis by weakening the LAB cell wall can improve the efficiency of LAB as antigen-delivery vectors in immune system stimulation efforts [12]. More recently, it has been proposed that bacterial surface adhesins could favor the persistence of probiotic bacteria in the gastrointestinal tract [13]. Also, cell wall microbe-associated molecular patterns (MAMPs) identified in pathogens could play a role in the cross-talk that takes place between commensal or probiotic bacteria and their hosts [14,15]. As predicted by Delcour et al. [16], the availability of whole genome sequences has boosted research on LAB cell wall structure and function over the last fifteen years. Here, we review the current state of knowledge on the structure and function of the cell wall components (PG, TAs, PSs, and proteins) of the most investigated LAB, including Lactococcus lactis and several lactobacilli, mainly Lactobacillus plantarum, Lactobacillus casei, and Lactobacillus rhamnosus. Page 2 of 23 Gram-negative bacteria but which is also present in L. plantarum. In other LAB, the Lys-type PG is found and includes an interpeptide bridge made of one D-amino acid (e.g., D-Asp or D-Asn in L. lactis, L. casei, and most lactobacilli) (Figure 1) or several L-amino acids (e.g., L-Ala 2 or L-Ala 3 in Streptococcus thermophilus) [17]. PG peptide chains connected by 3-3 cross-links, which predominate in Mycobacterium tuberculosis [18] and in Clostridium difficile [19], have not been described in LAB to date. Although a given bacterial species has a basic, characteristic PG structure, the PG layer remains in a dynamic state throughout a bacterium’s life, and PG structure is the result of complex biosynthetic, maturation, and degradation reactions, which will be described (...truncated)