Media Ion Composition Controls Regulatory and Virulence Response of Salmonella in Spaceflight

Wilson, James W.; Ott, C. Mark; Quick, Laura; Davis, Richard R.; Bentrup, Kerstin Höner zu; Crabbé, Aurélie; Richter, Emily; Sarker, Shameema; Barrila, Jennifer; Porwollik, Steffen; Cheng, Pui; McClelland, Michael; Tsaprailis, George; Radabaugh, Timothy; Hunt, Andrea; Shah, Miti; Nelman-Gonzalez, Mayra; Hing, Steve; Parra, Macarena; Dumars, Paula; Norwood, Kelly L.; Bober, Ramona; Devich, Jennifer; Ruggles, Ashleigh; Cdebaca, Autumn; Narayan, Satro; Benjamin, J. D.; Goulart, Carla; Rupert, Mark; Catella, Luke; Schurr, Michael J.; Buchanan, Kent L.; Morici, Lisa A.; McCracken, James; Porter, Marc D.; Pierson, Duane L.; Smith, Scott M.; Mergeay, Max; Leys, Natalie; Stefanyshyn-Piper, Heidemarie M.; Gorie, Dominic; Nickerson, Cheryl A.

doi:10.1371/journal.pone.0003923

Cited by 137 publications

(180 citation statements)

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“…Several studies already reported a more apparent bacterial response when cultivation in space flight, and space flight analogs was performed on rich medium Leff, 2004, 2006;Benoit and Klaus, 2007;Wilson et al, 2008). However, the difference in growth medium composition is probably not the only factor responsible for the difference in expression pattern for MESSAGE 2 and BASE-A.…”

Section: Discussionmentioning

confidence: 98%

“…Indeed, numerous in-flight studies have confirmed that space flight can have a pronounced effect on a variety of microbial parameters including changes in microbial proliferation rate, cell morphology, cell physiology, cell metabolism, genetic transfer among cells and viral reactivation within the cells (reviewed in Leys et al, 2004;Nickerson et al, 2004;Nicholson et al, 2005;Klaus and Howard, 2006). However, previous studies have also shown that the results from space flight and space flight analog experiments can radically differ when using different bacteria or when using the same bacterium but different culture media Leff, 2004, 2006;Benoit and Klaus, 2007;Wilson et al, 2008;Leys et al, in press).…”

Section: Introductionmentioning

confidence: 99%

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Experimental design and environmental parameters affect Rhodospirillum rubrum S1H response to space flight

et al. 2009

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In view of long-haul space exploration missions, the European Space Agency initiated the MicroEcological Life Support System Alternative (MELiSSA) project targeting the total recycling of organic waste produced by the astronauts into oxygen, water and food using a loop of bacterial and higher plant bioreactors. In that purpose, the a-proteobacterium, Rhodospirillum rubrum S1H, was sent twice to the International Space Station and was analyzed post-flight using a newly developed R. rubrum whole genome oligonucleotide microarray and high throughput gel-free proteomics with Isotope-Coded Protein Label technology. Moreover, in an effort to identify a specific response of R. rubrum S1H to space flight, simulation of microgravity and space-ionizing radiation were performed on Earth under identical culture set-up and growth conditions as encountered during the actual space journeys. Transcriptomic and proteomic data were integrated and permitted to put forward the importance of medium composition and culture set-up on the response of the bacterium to space flight-related environmental conditions. In addition, we showed for the first time that a low dose of ionizing radiation (2 mGy) can induce a significant response at the transcriptomic level, although no change in cell viability and only a few significant differentially expressed proteins were observed. From the MELiSSA perspective, we could argue the effect of microgravity to be minimized, whereas R. rubrum S1H could be more sensitive to ionizing radiation during long-term space exploration mission.

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Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Experimental design and environmental parameters affect Rhodospirillum rubrum S1H response to space flight

et al. 2009

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“…Biodegradation of critical materials can result in system failures that may endanger crews. Evidence gained during the SSP suggests that infectious diseases and allergic responses may increase on long exploration missions due to sustained immune deficiencies (11)(12)(13)(14)(15) and increased virulence of some microorganism (7)(8)(9)(10). …”

Section: Identification Of Microbiological Hazards and Risksmentioning

confidence: 99%

“…Our understanding of the effects of spaceflight on these life forms was greatly enhanced during the Space Shuttle Program (SSP). Some bacteria and fungi were shown to be more virulent as a result of spaceflight (7)(8)(9)(10). Immune studies showed decreases in innate immunity, cell mediated immunity (11)(12)(13)(14)(15), and increased latent virus reactivation (16)(17)(18)(19).…”

Section: Introductionmentioning

confidence: 99%

Microbiological Lessons Learned From the Space Shuttle

Pierson

Ott

Bruce³

et al. 2011

41st International Conference on Environmental Systems

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“…In these studies, microarray analysis revealed that S. Typhimurium iprA was upregulated in cultures inoculated and grown during spaceflight (compared to identically grown ground controls) and in cultures grown under low-fluid-shear RWV conditions (compared to RWV controls in which low-fluid-shear conditions were disrupted) (6,7). Interestingly, both spaceflight and RWV growth conditions increase the virulence of S. Typhimurium assayed using murine infection models (6,9,10). However, to our knowledge, the iprA gene is uncharacterized in the literature beyond these observations.…”

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The Bacterial iprA Gene Is Conserved across Enterobacteriaceae, Is Involved in Oxidative Stress Resistance, and Influences Gene Expression in Salmonella enterica Serovar Typhimurium

et al. 2016

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The iprA gene (formerly known as yaiV or STM0374) is located in a two-gene operon in the Salmonella enterica serovar Typhimurium genome and is associated with altered expression during spaceflight and rotating-wall-vessel culture conditions that increase virulence. However, iprA is uncharacterized in the literature. In this report, we present the first targeted characterization of this gene, which revealed that iprA is highly conserved across Enterobacteriaceae. We found that S. Typhimurium, Escherichia coli, and Enterobacter cloacae ⌬iprA mutant strains display a multi-log-fold increase in oxidative stress resistance that is complemented using a plasmid-borne wild-type (WT) copy of the S. Typhimurium iprA gene. This observation was also associated with increased catalase activity, increased S. Typhimurium survival in macrophages, and partial dependence on the katE gene and full dependence on the rpoS gene. Our results indicate that IprA protein activity is sensitive to deletion of the N-and C-terminal 10 amino acids, while a region that includes amino acids 56 to 80 is dispensable for activity. RNA sequencing (RNA-Seq) analysis revealed several genes altered in expression in the S. Typhimurium ⌬iprA mutant strain compared to the WT, including those involved in fimbria formation, spvABCD-mediated virulence, ethanolamine utilization, the phosphotransferase system (PTS) transport, and flagellin phase switching from FlgB to FliC (likely a stochastic event) and several genes of hypothetical or putative function. IMPORTANCEOverall, this work reveals that the conserved iprA gene measurably influences bacterial biology and highlights the pool of currently uncharacterized genes that are conserved across bacterial genomes. These genes represent potentially useful targets for bacterial engineering, vaccine design, and other possible applications.M any large-scale genomic studies, virulence factor identification assays, and whole-genome expression analyses have revealed bacterial genes that are uncharacterized but are associated with gene expression changes in different environments that can affect virulence and stress survival (see references 1-8 and several others). These studies reveal a pool of genes that are not understood or characterized but whose importance is highlighted due to how they were identified and, in some cases, to high conservation across bacterial genomes. The iprA gene (previously known as yaiV or STM0374) is located in a two-gene operon in the Salmonella enterica serovar Typhimurium genome and has been observed to display altered expression during spaceflight and under rotating-wall-vessel (RWV) culture conditions, which increase virulence (6, 7). In these studies, microarray analysis revealed that S. Typhimurium iprA was upregulated in cultures inoculated and grown during spaceflight (compared to identically grown ground controls) and in cultures grown under low-fluid-shear RWV conditions (compared to RWV controls in which low-fluid-shear conditions were disrupted) (6, 7). Interestingly, bot...

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Media Ion Composition Controls Regulatory and Virulence Response of Salmonella in Spaceflight

Cited by 137 publications

References 30 publications

Experimental design and environmental parameters affect Rhodospirillum rubrum S1H response to space flight

Experimental design and environmental parameters affect Rhodospirillum rubrum S1H response to space flight

Microbiological Lessons Learned From the Space Shuttle

The Bacterial iprA Gene Is Conserved across Enterobacteriaceae, Is Involved in Oxidative Stress Resistance, and Influences Gene Expression in Salmonella enterica Serovar Typhimurium

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