The Effect of Oxygen on Bile Resistance in Listeria monocytogenes

Abstract

Listeria monocytogenes is a Gram-positive facultative anaerobe that is the causative agent of the disease listeriosis. The infectious ability of this bacterium is dependent upon resistance to stressors encountered within the gastrointestinal tract, including bile. Previous studies have indicated bile salt hydrolase activity increases under anaerobic conditions, suggesting anaerobic conditions influence stress responses. Therefore, the goal of this study was to determine if reduced oxygen availability increased bile resistance of L. monocytogenes. Four strains representing three serovars were evaluated for changes in viability and proteome expression following exposure to bile in aerobic or anaerobic conditions. Viability for F2365 (serovar 4b), EGD-e (serovar 1/2a), and 10403S (serovar 1/2a) increased following exposure to 10% porcine bile under anaerobic conditions (P < 0.05). However, HCC23 (serovar 4a) exhibited no difference (P > 0.05) in bile resistance between aerobic and anaerobic conditions, indicating that oxygen availability does not influence resistance in this strain. The proteomic analysis indicated F2365 and EGD-e had an increased expression of proteins associated with cell envelope and membrane bioenergetics under anaerobic conditions, including thioredoxin-disulfide reductase and cell division proteins. Interestingly, HCC23 had an increase in several dehydrogenases following exposure to bile under aerobic conditions, suggesting that the NADH:NAD+ is altered and may impact bile resistance. Variations were observed in the expression of the cell shape proteins between strains, which corresponded to morphological differences observed by scanning electron microscopy. These data indicate that oxygen availability influences bile resistance. Further research is needed to decipher how these changes in metabolism impact pathogenicity in vivo and also the impact that this has on susceptibility of a host to listeriosis.

The Listeria monocytogenes Bile Stimulon under Acidic Conditions Is Characterized by Strain-Specific Patterns and the Upregulation of Motility, Cell Wall Modification Functions, and the PrfA Regulon

“…While a previous proteomic study of L. monocytogenes (Payne et al, 2013 ) identified alterations in levels of proteins associated with DNA repair, chaperone activity, and oxidative stress response in response to bile exposure under anaerobic and neutral pH conditions, it did not detail either a pan or core bile stimulon (Payne et al, 2013 ). Similarly, a more recent proteomic study also identified a number of genes induced in L. monocytogenes in response to bile stress under neutral pH aerobic and anaerobic conditions, but did not detail an overall bile stimulon (Wright et al, 2016 ). However, a transcriptomic study of the bile regulon for L. monocytogenes 10403S, also using bile exposure at neutral pH (Quillin et al, 2011 ), confirmed a large rearrangement of the transcriptomic landscape after bile exposure with 391 differentially expressed genes after bile exposure; similar to our findings this response was characterized by up-regulation of many cellular processes including cell wall processes and transport related functions.…”

“…However, once bile is released into the duodenum postprandially, it becomes active in this low pH environment (Dowd et al, 2011 ). Previous proteomic and transcriptomic studies of the L. monocytogenes bile stimulon have been performed under aerobic and anaerobic conditions but at neutral pH (Quillin et al, 2011 ; Payne et al, 2013 ; Wright et al, 2016 ). To better understand the response of L. monocytogenes to conditions encountered in the proximal part of the small intestine, we characterized the transcriptomic response triggered by exposure to 1.1% bile in an acidic (pH 5.5) environment in two strains of L. monocytogenes representing lineages I and II.…”

Mucosal Infections and Invasive Potential of Nonencapsulated Streptococcus pneumoniae Are Enhanced by Oligopeptide Binding Proteins AliC and AliD

“…Strain MNZ41 and JLB01 proteomes were evaluated using differential expression analysis based on peptide precursor mass ion current performed using the Perl programing language as described previously ( 55 ). Briefly, for each identified peptide, elution curves were integrated and organized by protein and then technical replicate.…”

Protective Microbiota: From Localized to Long-Reaching Co-Immunity

“…Secondary bile acids inhibit the germination and growth of C. difficile in the colon. Bile acids are released and mostly reabsorbed upstream in the small intestine, decreasing greatly in concentration further downstream ( 227 , 228 ). However, small intestinal microbiota can inhibit re-absorption by deconjugating bile acids, thus promoting their excretion down and out of the large intestine ( 229 ).…”