1] Department of Microbiology and Molecular Genetics, 6180 Biomedical Physical Sciences, Michigan State University, East Lansing, Michigan 48824, USA.  Department of Internal Medicine, University of Michigan, Ann Arbor, Michigan 48109, USA.
Competition for molecular oxygen (O(2)) among respiratory microorganisms is intense because O(2) is a potent electron acceptor. This competition leads to the formation of microoxic environments wherever microorganisms congregate in aquatic, terrestrial and host-associated communities. Bacteria can harvest O(2) present at low, even nanomolar, concentrations using high-affinity terminal oxidases. Here, we report the results of surveys searching for high-affinity terminal oxidase genes in sequenced bacterial genomes and shotgun metagenomes. The results indicate that bacteria with the potential to respire under microoxic conditions are phylogenetically diverse and intriguingly widespread in nature. We explore the implications of these findings by highlighting the importance of microaerobic metabolism in host-associated bacteria related to health and disease.
"The gut microbiota of healthy individuals is dominated by anaerobic bacteria, which outnumber aerobic and facultative anaerobic bacteria by a factor of 100–1,000:1 (Quigley and Quera, 2006), while the root microbiota is enriched for Proteobacteria, a phylum dominated by aerobic species. Consistent with this, genes encoding high-affinity oxidases that use O 2 as a terminal electron acceptor are overrepresented in gut metagenomes, whereas those encoding low-affinity oxidases are enriched in soil metagenomes (Morris and Schmidt, 2013). "
"In the environment, microbial communities are known to stratify based on oxygen and other chemical gradients (Fenchel and Finlay, 2008; Morris and Schmidt, 2013). CF mucus also contains oxygen gradients (Worlitzsch et al., 2002; Morris and Schmidt, 2013), suggesting that microbes may stratify similarly. Thus the micro-environment of a mucus-filled bronchiole can be considered analogous to the Winogradsky column, developed by Sergei Winogradsky to study the stratification of microbial communities in sediment based on chemical and oxygen gradients (Winogradsky, 1897). "
[Show abstract][Hide abstract] ABSTRACT: There is a poor understanding of how the physiology of polymicrobial communities in cystic fibrosis (CF) lungs contributes to pulmonary exacerbations and lung function decline. In this study, a microbial culture system based on the principles of the Winogradsky column (WinCF system) was developed to study the physiology of CF microbes. The system used glass capillary tubes filled with artificial sputum medium to mimic a clogged airway bronchiole. Chemical indicators were added to observe microbial physiology within the tubes. Characterization of sputum samples from seven patients showed variation in pH, respiration, biofilm formation and gas production, indicating that the physiology of CF microbial communities varied among patients. Incubation of homogenized tissues from an explant CF lung mirrored responses of a Pseudomonas aeruginosa pure culture, supporting evidence that end-stage lungs are dominated by this pathogen. Longitudinal sputum samples taken through two exacerbation events in a single patient showed that a two-unit drop in pH and a 30% increase in gas production occurred in the tubes prior to exacerbation, which was reversed with antibiotic treatment. Microbial community profiles obtained through amplification and sequencing of the 16S rRNA gene showed that fermentative anaerobes became more abundant during exacerbation and were then reduced during treatment where P. aeruginosa became the dominant bacterium. Results from the WinCF experiments support the model where two functionally different CF microbial communities exist, the persistent Climax Community and the acute Attack Community. Fermentative anaerobes are hypothesized to be the core members of the Attack Community and production of acidic and gaseous products from fermentation may drive developing exacerbations. Treatment targeting the Attack Community may better resolve exacerbations and resulting lung damage.
The ISME Journal 12/2014; 9(4). DOI:10.1038/ismej.2014.234 · 9.30 Impact Factor
"Not all organisms are capable of carrying out respiration in variable oxygen gradient conditions. Some microbes span the microaerophilic to aerotolerant niches and, within an environment, the successional community structure based on available terminal electron acceptors should structure the community-level respiratory processes (Morris and Schmidt, 2013). Microbes drive biogeochemical reactions and are paramount in nutrient cycling. "
[Show abstract][Hide abstract] ABSTRACT: Intense annual spring phytoplankton blooms and thermohaline stratification lead to anoxia in Chesapeake Bay bottom waters. Once oxygen becomes depleted in the system, microbial communities use energetically favorable alternative electron acceptors for respiration. The extent to which changes in respiration are reflected in community gene expression have only recently been investigated. Metatranscriptomes prepared from near-bottom water plankton over a four month time series in central Chesapeake Bay demonstrated changes consistent with terminal electron acceptor availability. The frequency of respiration-related genes in metatranscriptomes was examined by BLASTx against curated databases of genes intimately and exclusively involved in specific electron acceptor utilization pathways. The relative expression of genes involved in denitrification and dissimilatory nitrate reduction to ammonium were coincident with changes in nitrate, nitrite and ammonium concentrations. Dissimilatory iron and manganese reduction transcript ratios increase during anoxic conditions and corresponded with the highest soluble reactive phosphate and manganese concentrations. The sulfide concentration peaked in late July and early August and also matched dissimilatory sulfate reduction transcript ratios. We show that rather than abrupt transitions between terminal electron acceptors, there seems to be substantial overlap in time and space of these various anaerobic respiratory processes in Chesapeake Bay.
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