{"title":"Oxygen tolerance in anaerobes as a virulence factor and a health-beneficial property","authors":"Lyudmila Boyanova , Liliya Boyanova , Petyo Hadzhiyski , Raina Gergova , Rumyana Markovska","doi":"10.1016/j.anaerobe.2024.102897","DOIUrl":null,"url":null,"abstract":"<div><p>Oxygen tolerance of anaerobes is a virulence factor, but can also be a beneficial property. Many species have evolved to tolerate or take advantage of the presence of low, especially nanaerobic (≤0.14 %) oxygen concentrations. Oxygen tolerance is genus-, species- and strain-dependent according to their protective mechanisms. It was better expressed in some pathogenic species such as <em>Bacteroides fragilis, Clostridioides difficile</em>, and <em>Clostridium perfringens,</em> as well as in <em>Akkermansia muciniphila</em> than in other potential probiotics such as <em>Alistipes, Blautia</em> and <em>Roseburia</em> spp. Different degrees of oxygen sensitivity were found between the strains of <em>Anaerostipes, Faecalibacterium,</em> and <em>Bifidobacterium</em> spp. Importantly, clostridial spores and anaerobes in biofilms are protected from oxidation. Rubrerythrins and flavodiiron proteins and two regulators (sigma factor B and PerR) contribute to <em>C. difficile</em> protection from reactive oxygen species (ROS). The frequent pathogen, <em>B. fragilis,</em> has numerous protective factors such as enzymes (catalase, superoxide dismutase, alkyl hydroperoxidase, thioredoxin peroxidase, and aerobic-type NrdAB ribonucleotide reductase), and nanaerobic respiration. Seven proteins confer strain-specific oxygen adaptation of <em>Faecalibacterium prausnitzii</em>. Oxygen tolerance protects anaerobes from ROS, shields their DNA and modulates gene expression. Furthermore, oxygen can induce mutations leading to antibiotic resistance as shown in <em>Prevotella melaninogenica</em>. Some <em>Faecalibacterium, Anaerostipes, Bifidobacterium,</em> and <em>Akkermansia</em> strains from the intestinal microbiota exhibiting oxygen tolerance may become next-generation probiotic candidates. Further studies are needed to reveal oxygen effects on more anaerobic species and strains, and the influence of oxygen on antibiotic resistance. More studies on oxygen-tolerant probiotic strains can be useful to optimize biotechnological methods.</p></div>","PeriodicalId":8050,"journal":{"name":"Anaerobe","volume":"89 ","pages":"Article 102897"},"PeriodicalIF":2.5000,"publicationDate":"2024-08-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Anaerobe","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1075996424000805","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Oxygen tolerance of anaerobes is a virulence factor, but can also be a beneficial property. Many species have evolved to tolerate or take advantage of the presence of low, especially nanaerobic (≤0.14 %) oxygen concentrations. Oxygen tolerance is genus-, species- and strain-dependent according to their protective mechanisms. It was better expressed in some pathogenic species such as Bacteroides fragilis, Clostridioides difficile, and Clostridium perfringens, as well as in Akkermansia muciniphila than in other potential probiotics such as Alistipes, Blautia and Roseburia spp. Different degrees of oxygen sensitivity were found between the strains of Anaerostipes, Faecalibacterium, and Bifidobacterium spp. Importantly, clostridial spores and anaerobes in biofilms are protected from oxidation. Rubrerythrins and flavodiiron proteins and two regulators (sigma factor B and PerR) contribute to C. difficile protection from reactive oxygen species (ROS). The frequent pathogen, B. fragilis, has numerous protective factors such as enzymes (catalase, superoxide dismutase, alkyl hydroperoxidase, thioredoxin peroxidase, and aerobic-type NrdAB ribonucleotide reductase), and nanaerobic respiration. Seven proteins confer strain-specific oxygen adaptation of Faecalibacterium prausnitzii. Oxygen tolerance protects anaerobes from ROS, shields their DNA and modulates gene expression. Furthermore, oxygen can induce mutations leading to antibiotic resistance as shown in Prevotella melaninogenica. Some Faecalibacterium, Anaerostipes, Bifidobacterium, and Akkermansia strains from the intestinal microbiota exhibiting oxygen tolerance may become next-generation probiotic candidates. Further studies are needed to reveal oxygen effects on more anaerobic species and strains, and the influence of oxygen on antibiotic resistance. More studies on oxygen-tolerant probiotic strains can be useful to optimize biotechnological methods.
期刊介绍:
Anaerobe is essential reading for those who wish to remain at the forefront of discoveries relating to life processes of strictly anaerobes. The journal is multi-disciplinary, and provides a unique forum for those investigating anaerobic organisms that cause infections in humans and animals, as well as anaerobes that play roles in microbiomes or environmental processes.
Anaerobe publishes reviews, mini reviews, original research articles, notes and case reports. Relevant topics fall into the broad categories of anaerobes in human and animal diseases, anaerobes in the microbiome, anaerobes in the environment, diagnosis of anaerobes in clinical microbiology laboratories, molecular biology, genetics, pathogenesis, toxins and antibiotic susceptibility of anaerobic bacteria.