Inactivation and Gene Expression of a Virulent Wastewater <i>Escherichia coli</i> Strain and the Nonvirulent Commensal <i>Escherichia coli</i> DSM1103 Strain upon Solar Irradiation

Aljassim, Nada I.; Mantilla‐Calderon, David; Wang, Tiannyu; Hong, Pei‐Ying

doi:10.1021/acs.est.6b05377

Cited by 36 publications

(60 citation statements)

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“…Additionally, the ranges of relative expression ratios determined here (minimum, R ϭ 0.5; maximum, R ϭ 4.4) are similar to expression levels in previous studies of E. faecalis in oligotrophic seawater systems (6, 7), which found maximum changes in expression of ϳ3-fold by microarray. In contrast, some previous studies have observed larger expression changes in E. coli after sunlight exposure, but we expect this may be due to either the use of growth medium during sunlight exposure (9) or the use of a different method (i.e., transcriptome sequencing [RNA-seq]) to detect gene expression changes (26). Despite the fact that large changes in expression were not detected here, the approximately stable expression levels across samples in both systems suggest that cells remain transcriptionally active, even after the majority of cells are not culturable.…”

Section: Discussionmentioning

confidence: 70%

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Staphylococcus aureus Strain Newman Photoinactivation and Cellular Response to Sunlight Exposure

McClary

Sassoubre

Boehm

2017

Appl Environ Microbiol

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Sunlight influences microbial water quality of surface waters. Previous studies have investigated photoinactivation mechanisms and cellular photostress responses of fecal indicator bacteria (FIB), including Escherichia coli and enterococci, but further work is needed to characterize photostress responses of bacterial pathogens. Here we investigate the photoinactivation of Staphylococcus aureus (strain Newman), a pigmented, waterborne pathogen of emerging concern. We measured photodecay using standard culture-based assays and cellular membrane integrity and investigated photostress response by measuring the relative number of mRNA transcripts of select oxidative stress, DNA repair, and metabolism genes. Photoinactivation experiments were performed in both oxic and anoxic systems to further investigate the role of oxygen-mediated and non-oxygen-mediated photoinactivation mechanisms. S. aureus lost culturability much faster in oxic systems than in anoxic systems, indicating an important role for oxygen in photodecay mechanisms. S. aureus cell membranes were damaged by sunlight exposure in anoxic systems but not in oxic systems, as measured by cell membrane permeability to propidium iodide. After sunlight exposure, S. aureus increased expression of a gene coding for methionine sulfoxide reductase after 12 h of sunlight exposure in the oxic system and after 6 h of sunlight exposure in the anoxic system, suggesting that methionine sulfoxide reductase is an important enzyme for defense against both oxygen-dependent and oxygen-independent photostresses. This research highlights the importance of oxygen in bacterial photoinactivation in environmentally relevant systems and the complexity of the bacterial photostress response with respect to cell structure and transcriptional regulation.IMPORTANCE Staphylococcus aureus is a pathogenic bacterium that causes gastrointestinal, respiratory, and skin infections. In severe cases, S. aureus infection can lead to life-threatening diseases, including pneumonia and sepsis. Cases of communityacquired S. aureus infection have been increasing in recent years, pointing to the importance of considering S. aureus transmission pathways outside the hospital environment. Associations have been observed between recreational water contact and staphylococcal skin infections, suggesting that recreational waters may be an important environmental transmission pathway for S. aureus. However, prediction of human health risk in recreational waters is hindered by incomplete knowledge of pathogen sources, fate, and transport in this environment. This study is an in-depth investigation of the inactivation of a representative strain of S. aureus by sunlight exposure, one of the most important factors controlling the fate of microbial contaminants in clear waters, which will improve our ability to predict water quality changes and human health risk in recreational waters.KEYWORDS Staphylococcus aureus, coastal waters, enterococci, fecal indicator bacteria, photoinactivation

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Section: Discussionmentioning

confidence: 70%

“…Fewer studies have investigated photoinactivation mechanisms of bacterial pathogens in aquatic environments (13,(26)(27)(28). Previous studies have identified factors and characteristics associated with increased photoinduced damage of FIB.…”

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confidence: 99%

Staphylococcus aureus Strain Newman Photoinactivation and Cellular Response to Sunlight Exposure

McClary

Sassoubre

Boehm

2017

Appl Environ Microbiol

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“…Recent ndings also suggest that ARB cells themselves may be more resistant to inactivation during solar irradiation than cells of non-resistant strains, possibly due to upregulation in expression of a wider array of stress response and repair genes in ARB than in non-resistant strains. 209 Even if ARB cells are effectively inactivated by solar irradiation, their ARG-containing DNA may remain intact and capable of transferring resistance traits to non-resistant bacteria. A challenge with assessing this risk is that ARGs detected by qPCR may no longer be capable of transferring resistance via transformation.…”

Section: 208mentioning

confidence: 99%

Sunlight-mediated inactivation of health-relevant microorganisms in water: a review of mechanisms and modeling approaches

Nelson

Boehm

Davies‐Colley

et al. 2018

Environ. Sci.: Processes Impacts

207

221

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Health-relevant microorganisms present in natural surface waters and engineered treatment systems that are exposed to sunlight can be inactivated by a complex set of interacting mechanisms. The net impact of sunlight depends on the solar spectral irradiance, the susceptibility of the specific microorganism to each mechanism, and the water quality; inactivation rates can vary by orders of magnitude depending on the organism and environmental conditions. Natural organic matter (NOM) has a large influence, as it can attenuate radiation and thus decrease inactivation by endogenous mechanisms. Simultaneously NOM sensitizes the formation of reactive intermediates that can damage microorganisms via exogenous mechanisms. To accurately predict inactivation and design engineered systems that enhance solar inactivation, it is necessary to model these processes, although some details are not yet sufficiently well understood. In this critical review, we summarize the photo-physics, -chemistry, and -biology that underpin sunlight-mediated inactivation, as well as the targets of damage and cellular responses to sunlight exposure. Viruses that are not susceptible to exogenous inactivation are only inactivated if UVB wavelengths (280-320 nm) are present, such as in very clear, open waters or in containers that are transparent to UVB. Bacteria are susceptible to slightly longer wavelengths. Some viruses and bacteria (especially Gram-positive) are susceptible to exogenous inactivation, which can be initiated by visible as well as UV wavelengths. We review approaches to model sunlightmediated inactivation and illustrate how the environmental conditions can dramatically shift the inactivation rate of organisms. The implications of this mechanistic understanding of solar inactivation are discussed for a range of applications, including recreational water quality, natural treatment systems, solar disinfection of drinking water (SODIS), and enhanced inactivation via the use of sensitizers and photocatalysts. Finally, priorities for future research are identified that will further our understanding of the key role that sunlight disinfection plays in natural systems and the potential to enhance this process in engineered systems. Environmental signicanceThe manuscript provides a comprehensive synthesis of the current understanding of the mechanisms by which sunlight causes damage to microorganisms, ultimately leading to inactivation. This topic is important for understanding the fate and transport of microbiological contaminants in all sunlit surface waters, including fresh and marine ecosystems, as well as engineered treatment systems.

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“…Indeed, the same E. coli PI7 was observed to upregulate transcriptional responses of genes related to persister cell formation upon solar irradiation (45), suggesting that E. coli PI7 adopts this strategy to facilitate its persistence during stressful conditions.…”

Section: Discussionmentioning

confidence: 99%

Fate and Persistence of a Pathogenic NDM-1-Positive Escherichia coli Strain in Anaerobic and Aerobic Sludge Microcosms

Mantilla‐Calderon

Hong

2017

Appl Environ Microbiol

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The presence of emerging biological pollutants in treated wastewater effluents has gained attention due to increased interest in water reuse. To evaluate the effectiveness of the removal of such contaminants by the conventional wastewater treatment process, the fate and decay kinetics of NDM-1-positive Escherichia coli strain PI7 and its plasmid-encoded antibiotic resistance genes (ARGs) were assessed in microcosms of anaerobic and aerobic sludge. Results showed that E. coli PI7 decayed at a significantly lower rate under anaerobic conditions. Approximate half-lives were 32.4 ± 1.4 h and 5.9 ± 0.9 h in the anaerobic and aerobic microcosms, respectively. In the aerobic microcosms, after 72 h of operation, E. coli PI7 remained detectable, but no further decay was observed. Instead, 1 in every 10,000 E. coli cells was identified to be recalcitrant to decay and persist indefinitely in the sludge. ARGs associated with the E. coli PI7 strain were detected to have transferred to other native microorganisms in the sludge or were released to the liquid fraction upon host decay. Extracellular DNA quickly degraded in the liquid fraction of the aerobic sludge. In contrast, no DNA decay was detected in the anaerobic sludge water matrix throughout the 24-h sampling period. This study suggests an increased likelihood of environmental dispersion of ARGs associated with anaerobically treated wastewater effluents and highlights the potential importance of persister cells in the dissemination of E. coli in the environment during reuse events of treated wastewater.IMPORTANCE This study examines the decay kinetics of a pathogenic and antibiotic resistant strain of Escherichia coli in microcosms simulating biological treatment units of aerobic and anaerobic sludge. The results of this study point at a significantly prolonged persistence of the E. coli and the associated antibiotic resistance gene in the anaerobic sludge. However, horizontal transfer of the plasmid encoding the antibiotic resistance gene was detected in the aerobic sludge by a cultivation method. A subpopulation of persister E. coli cells was also detected in the aerobic sludge. The findings of this study suggest potential areas of concern arising from pathogenic and antibiotic-resistant E. coli during both anaerobic and aerobic sludge treatment processes.

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Inactivation and Gene Expression of a Virulent Wastewater Escherichia coli Strain and the Nonvirulent Commensal Escherichia coli DSM1103 Strain upon Solar Irradiation

Cited by 36 publications

References 62 publications

Staphylococcus aureus Strain Newman Photoinactivation and Cellular Response to Sunlight Exposure

Staphylococcus aureus Strain Newman Photoinactivation and Cellular Response to Sunlight Exposure

Sunlight-mediated inactivation of health-relevant microorganisms in water: a review of mechanisms and modeling approaches

Fate and Persistence of a Pathogenic NDM-1-Positive Escherichia coli Strain in Anaerobic and Aerobic Sludge Microcosms

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