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Electron Transport Chains of Lactic Acid Bacteria

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Electron Transport Chains of Lactic Acid Bacteria Electron Transport Chains of Lactic Acid Bacteria Rob J.W. Brooijmans Promotor: Prof. dr. Willem M. de Vos, hoogleraar Microbiologie Co-promotor: Prof. dr. Jeroen Hugenholtz, hoogleraar Industriele Moleculaire Microbiologie (Universiteit van Amsterdam) Promotiecommissie: Prof. dr. P. Hols (Université de Catholique de Louvain) Dr. E. Johansen (Chr. Hansen, Denmark) Prof. dr. T. Abee (Wageningen University) Prof. dr. M. J. Teixeira de Mattos (University of Amsterdam) Dit onderzoek is uitgevoerd binnen “The Graduate School VLAG” Electron Transport Chains of Lactic Acid Bacteria Rob J.W. Brooijmans Proefschrift ter verkrijging van de graad van doctor op gezag van de rector magnificus van Wageningen Universiteit Prof. dr. M. J. Kropff in het openbaar te verdedigen op 10 november 2008 des namiddags te vier uur in de Aula R. J. W. Brooijmans (2008) Electron Transport Chains of Lactic Acid Bacteria Thesis Wageningen University – with summary in Dutch Source cover-photo: NASA ISBN 978-90-8585-302-2 Contents Abstract 1 Chapter 1 Introduction and Outline of thesis 3 Chapter 2 Generation of a membrane potential by Lactococcus 33 lactis through aerobic electron transport Chapter 3 Heme and menaquinone induced electron transport in 57 lactic acid bacteria Chapter 4 The electron transport chains of Lactobacillus 85 plantarum WCFS1 Chapter 5 Heme and menaquinone induced aerobic response in 111 Lactobacillus plantarum WCFS1 Chapter 6 The anaerobic electron transport chain of 131 Lactobacillus plantarum is an efficient redox sink Chapter 7 The electron transport chains of anaerobic prokaryotic 149 bacteria Chapter 8 General discussion and future perspectives 197 Samenvatting Nederlands 215 Dankwoord 221 About the author 223 List of publications 225 Training and Supervision Plan (VLAG) 227 Abstract Lactic acid bacteria are generally considered facultative anaerobic obligate fermentative bacteria. They are unable to synthesize heme. Some lactic acid bacteria are unable to form menaquinone as well. Both these components are cofactors of respiratory (electron transport) chains of prokaryotic bacteria. Lactococcus lactis, and several other lactic acid bacteria, however respond to the addition of heme in aerobic growth conditions. This response includes increased biomass and robustness. In this study we demonstrate that heme-grown Lactococcus lactis in fact do have a functional electron transport chain that is capable of generating a proton motive force in the presence of oxygen. In other words, heme addition induces respiration in Lactococcus lactis. This aerobic electron transport chain contains a NADH-dehydrogenase, a menaquinone-pool and a bd-type cytochrome. A phenotypic and genotypic screening revealed a similar response, induced by heme (and menaquinone) supplementation, in other lactic acid bacteria. The genome of Lactobacillus plantarum WCFS1 was predicted to encode a nitrate reductase A complex. We have found that Lactobacillus plantarum is capable of using nitrate as terminal electron acceptor, when heme and menaquinone are provided. Nitrate can be used by Lactobacillus plantarum as effective electron sink and allows growth on a extended range of substrates. The impact of both the aerobic and anaerobic electron transport chain, on the metabolism and global transcriptome of Lactobacillus plantarum were studied in detail. This work has resulted in the discovery of novel electron transport chains and respiratory capabilities of lactic acid bacteria. The potential respiratory capabilities of other, previously considered (strictly) anaerobic prokaryotic bacteria, were reviewed. 1 2 Chapter 1 Introduction and outline of thesis 3 Chapter 1 - Introduction Introduction This chapter will introduce the reader to lactic acid bacteria (LAB), general concepts of respiration and electron transport chains. Firstly, the general features, applications, fermentative metabolism and the main current research topics will be described. The second part will focus on bacterial respiration with a particular emphasis on Escherichia coli as model organism. Then the scientific observations are presented that have suggested heme- induced aerobic respiration in several LAB, such as Lactooccus lactis and Enterococcus faecalis. The introduction concludes with the outline of this thesis. 4 The Lactic acid bacteria The LAB are defined here as belonging to the order Lactobacillales, a related group of prokaryotic bacteria that are descended from a common ancestor (Fig. 1) Enterococcus faecalis Lactococcus lactis subsp. lactis Lactococcus lactis subsp. cremoris Streptococcus mutans Streptococcus pneumoniae pathogenic Streptococci Streptococcus agalactiae LAB common ancestor Streptococcus pyogenes Streptococcus thermophilus Lactobacillus gasseri Lactobacillus johnsonii Lactobacillus delbrueckii Lactobacillus acidophilus Lactobacillus casei Lactobacillus sakei Lactobacillus brevis Pediococcus pentosaceus Lactobacillus plantarum Leuconostoc mesenteroides Oenococcus oeni Lactobacillus salivarius outgroup species Figure 1. Evolutionary relationship of LAB. The phylogenetic tree of Lactobacillales constructed on the basis of concatenated alignments of four subunits (α, ß, ß', and δ) of the DNA-dependent RNA polymerase (based on Makarova et. al.) (37). The length of the branches represents evolutionary distance. The members of this group share several physiological features and include Gram- positive, acid tolerant, non-spore forming, rod- or cocci-shaped bacteria that are able to ferment carbohydrates to (lactic) acids (59). LAB have been used for the fermentation of foods already since prehistoric times, and do so without the production of toxins, so that it can still be consumed, safely (Table 1). 5 Chapter 1 - Introduction Product Microorganisms Substrate Wine, beer Saccharomyces cerevisiae, LAB grapes, grain, hops Bread Saccharomyces cerevisiae, LAB wheat, rye, grains Cheddar cheese Lactococcus (cremoris, lactis), Leuconostoc milk Swiss type cheese Lactobacillus (delbrueckii, bulgaricus, helveticus) milk Mould- and smear Carnobacterium piscicola, Brevibacterium linens milk ripened cheeses Yoghurts Streptococcus thermophilus, Lactobacillus bulgaricus milk Kefir Lactococci, yeast, Lactobacillus kefir (and others) milk Fermented meats Pediococci, Staphylococci, various LAB pork, beef Lactococcus lactis, Leuconostoc mesenteroides, Sauerkraut cabbage Lactobacillus (brevis, plantarum, curvatus, sake) Aspergillus (oryzae, soyae), Lactobacilli, Soy sauce soy beans, wheat Zygosaccharomyces rouxii Enterococcus (mundtii, faecium), Lactococcus (cremoris, Vegetables vegetables lactis), Lactobacillus (casei, plantarum) Fish Carnobacterium (piscicola, divergens) fish Table 1. Examples of foods that use LAB for their production, taken from Ross et. al. (52). Several species are also able to produce anti-microbial compounds that in conjunction with the process of acidification inhibits growth of other spoilage, and possibly toxin-producing, bacteria or fungi (43). Fermentation thus increases the shelf-life of foods and can reduce the chance of spoilage. These attributes are especially of great importance in many third-world countries with lower hygiene standards. Historically, mankind has used LAB to ferment their foods, without knowledge of the existence of (these) bacteria. Fermented foods have increased levels of nutrients, such as vitamins, are sometimes easier to digest then the raw food-product, and have altered and enhanced flavor profiles (29, 33). Typical examples of centuries-old food fermentations that involve LAB are the production of many types of yoghurts and cheeses from milk. The discovery that these fermentation processes could be initiated by active inoculation of (fresh) milk, with old 6 batches of yoghurt and cheese, has inevitably led to a symbiosis between LAB and man that is still evolving. For example, nutrient rich food-environments contain many complex organic compounds, such as peptides, vitamins and other co-factors. This “free” availability of these compounds relieves the selective pressure on the bacteria to maintain the metabolic capacity to produces them. Many species of LAB have been completely sequenced and the evolutionary (adaptive) trends in gene loss and gain can be deduced from this information. The LAB in general show extensive adaptation to the nutrient rich food-environments with significant gene loss (Fig. 2). Figure 2. Progressive loss of genes as seen in the genomes of LAB indicate extensive specialization, taken from Makarova et.al. (37). The numbers of the LAB specific clusters of orthologous protein encoding genes, found in the species and inferred at the various nodes of speciation, are given, as well as the concomitant gain (+) and loss (-) events. Most striking is that they have lost many biosynthetic capacities (8). A clear example of this is that cultivation of LAB on chemically defined medium requires supplementation with a variety of amino acids (26, 68). 7 Chapter 1 - Introduction Main research topics of lactic acid bacteria LAB are also found in a wide variety of natural environments, such as plants. The research interest of LAB has however been rather anthropocentric. It has predominantly focused on isolates from (industrial) food-fermentations and the (human) gastrointestinal tract and on human and animal pathogens (1, 59). In fact the human body can be considered a natural habitat for some LABl species as well. The research focus of LAB falls into three broad categories: the relationship between their metabolic activity and the
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