Abstract
The response of microorganisms to the spaceflight environment has tremendous implications for the risk of infectious disease for astronauts. Seminal studies using Salmonella enterica serovar Typhimurium (S. Typhimurium) demonstrated that the organism’s virulence was altered in response to culture in either spaceflight or spaceflight analog environments. Furthermore, evaluation of global changes in transcriptomic and proteomic profiles in S. Typhimurium in response to culture in these environments indicated that many of the alterations in gene expression were regulated by the conserved chaperone protein, Hfq. To determine similarities in spaceflight and/or spaceflight analog-induced responses in other pathogens, extensive studies were performed using the opportunistic pathogen Pseudomonas aeruginosa. As with S. Typhimurium, P. aeruginosa cultured in either spaceflight or spaceflight analog conditions demonstrated diverse molecular genetic response profiles, including those associated with pathogenesis-related responses and the Hfq regulon. Collectively, these discoveries are providing novel insight into both the conserved and varied molecular genetic and phenotypic responses found in a wide variety of pathogens cultured in both spaceflight and spaceflight analog conditions. Interestingly, the low fluid-shear culture conditions of both spaceflight and spaceflight analog environments are relevant to those encountered by pathogens in certain regions of the human body during the natural course of infection. Hence, novel virulence strategies unveiled during spaceflight and spaceflight analog culture hold promise to safeguard crew health, and may aid the quest for novel therapeutics and vaccines against pathogens for the general public on Earth.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- C4-HSL:
-
N-Butanoyl-l-homoserine lactone
- CF:
-
Cystic fibrosis
- EPEC:
-
Enteropathogenic E. coli
- ETEC:
-
Enterotoxigenic E. coli
- Fur:
-
Ferric uptake regulator
- HARV:
-
High aspect ratio (or rotating) vessel
- ISS:
-
International Space Station
- LD:
-
Lethal dose
- LPS:
-
Lipopolysaccharide
- LSMMG:
-
Low-shear modeled microgravity
- MEED:
-
Microbial ecology evaluation device
- MMG:
-
Modeled microgravity
- NASA:
-
National Aeronautics and Space Administration
- OES:
-
Orbital Environmental Simulator
- RT-PCR:
-
Reverse transcriptase-polymerase chain reaction
- RWV:
-
Rotating wall vessel
- SMG:
-
Simulated microgravity
- STLV:
-
Slow turning lateral vessel
References
Abshire CF, Prasai K, Soto I, Shi R, Concha M, Baddoo M et al (2016) Exposure of Mycobacterium marinum to low-shear modeled microgravity: effect on growth, the transcriptome and survival under stress. NPJ Microgravity 2:16038
Allen CA, Galindo CL, Pandya U, Watson DA, Chopra AK et al (2007) Transcription profiles of Streptococcus pneumoniae grown under different conditions of normal gravitation. Acta Astronaut 60:433–444
Allen CA, Niesel DW, Torres AG (2008) The effects of low-shear stress on adherent-invasive Escherichia coli. Environ Microbiol 10:1512–1525
Altenburg SD, Nielsen-Preiss SM, Hyman LE (2008) Increased filamentous growth of Candida albicans in simulated microgravity. Genomics Proteomics Bioinformatics 6:42–50
Bajolet-Laudinat O, Girod-de Bentzmann S, Tournier JM, Madoulet C, Plotkowski MC, Chippaux C et al (1994) Cytotoxicity of Pseudomonas aeruginosa internal lectin PA-I to respiratory epithelial cells in primary culture. Infect Immun 62:4481–4487
Berry D, Volz PA (1979) Phosphate uptake in Saccharomyces cerevisiae Hansen wild type and phenotypes exposed to space flight irradiation. Appl Environ Microbiol 38:751–753
Bjarnsholt T, Jensen PO, Fiandaca MJ, Pedersen J, Hansen CR, Andersen CB et al (2009) Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr Pulmonol 44:547–558
Blake J (1973) A note on mucus shear rates. Respir Physiol 17:394–399
Bruce RJ, Ott CM, Skuratov VM, Pierson DL (2005) Microbial surveillance of potable water sources of the International Space Station. SAE Trans 114:283–292
Carvalho HM, Teel LD, Goping G, O’Brien AD (2005) A three-dimensional tissue culture model for the study of attach and efface lesion formation by enteropathogenic and enterohaemorrhagic Escherichia coli. Cell Microbiol 7:1771–1781
Castro VA, Trasher AN, Healy M, Ott CM, Pierson DL (2004) Microbial characterization during the early habitation of the International Space Station. Microb Ecol 47:119–126
Castro SL, Nelman-Gonzalez M, Nickerson CA, Ott CM (2011) Low fluid shear culture of Staphylococcus aureus induces attachment-independent biofilm formation and represses hfq expression. Appl Environ Microbiol 77(18):6368–6378
Chemani C, Imberty A, de Bentzmann S, Pierre M, Wimmerova M, Guery BP et al (2009) Role of LecA and LecB lectins in Pseudomonas aeruginosa-induced lung injury and effect of carbohydrate ligands. Infect Immun 77:2065–2075
Chopra V, Fadl AA, Sha J, Chopra S, Galindo CL, Chopra AK (2006) Alterations in the virulence potential of enteric pathogens and bacterial-host cell interactions under simulated microgravity conditions. J Toxicol Environ Health A 69:1345–1370
Crabbé A, De Boever P, Van Houdt R, Moors H, Mergeay M, Cornelis P (2008) Use of the rotating wall vessel technology to study the effect of shear stress on growth behaviour of Pseudomonas aeruginosa PA01. Environ Microbiol 10:2098–2110
Crabbé A, Pycke B, Van Houdt R, Monsieurs P, Nickerson C, Leys N et al (2010) Response of Pseudomonas aeruginosa PAO1 to low shear modelled microgravity involves AlgU regulation. Environ Microbiol 12:1545–1564
Crabbé A, Schurr MJ, Monsieurs P, Morici L, Schurr J, Wilson JW et al (2011) Transcriptional and proteomic responses of Pseudomonas aeruginosa PAO1 to spaceflight conditions involve Hfq regulation and reveal a role for oxygen. Appl Environ Microbiol 77:1221–1230
Crabbé A, Nielsen-Preiss SM, Woolley CM, Barrila J, Buchanan K et al (2013) Spaceflight enhances cell aggregation and random budding in Candida albicans. PLoS One 8(12):e80677
Curtiss R III, Wanda SY, Gunn BM, Zhang X, Tinge SA et al (2009) Salmonella enterica serovar Typhimurium strains with regulated delayed attenuation in vivo. Infect Immun 77(3):1071–1082
Curtiss R III, Xin W, Li Y, Kong W, Wanda SY et al (2010) New technologies in using recombinant attenuated Salmonella vaccine vectors. Crit Rev Immunol 30(3):255–270
Davey ME, Caiazza NC, O’Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027–1036
Dickson KJ (1991) Summary of biological spaceflight experiments with cells. ASGSB Bull 4:151–260
Dingemans J, Monsieurs P, Yu SH, Crabbé A, Förstner KU et al (2016) Effect of shear stress on Pseudomonas aeruginosa isolated from the cystic fibrosis lung. MBio 7(4). https://doi.org/10.1128/mBio.00813-16
Dong T, Schellhorn HE (2010) Role of RpoS in virulence of pathogens. Infect Immun 78:887–897
Gao Q, Fang A, Pierson DL, Mishra SK, Demain AL (2001) Shear stress enhances microcin B17 production in a rotating wall bioreactor, but ethanol stress does not. Appl Microbiol Biotechnol 56:384–387
Gilboa-Garber N, Mizrahi L, Garber N (1977) Mannose-binding hemagglutinins in extracts of Pseudomonas aeruginosa. Can J Biochem 55:975–981
Gottesman S (2004) The small RNA regulators of Escherichia coli: roles and mechanisms. Annu Rev Microbiol 58:303–328
Gottesman S, McCullen CA, Guillier M, Vanderpool CK, Majdalani N, Benhammou J et al (2006) Small RNA regulators and the bacterial response to stress. Cold Spring Harb Symp Quant Biol 71:1–11
Gueguinou N, Huin-Schohn C, Bascove M, Bueb JL, Tschirhart E, Legrand-Frossi C et al (2009) Could spaceflight-associated immune system weakening preclude the expansion of human presence beyond Earth’s orbit? J Leukoc Biol 86:1027–1038
Guisbert E, Rhodius VA, Ahuja N, Witkin E, Gross CA (2007) Hfq modulates the sigmaE-mediated envelope stress response and the sigma32-mediated cytoplasmic stress response in Escherichia coli. J Bacteriol 189:1963–1973
Hawkins WR, Ziegelschmid JF (1975) Clinical aspects of crew health. In: Johnson RS, Dietlein LF, Berry CA (eds) Biomedical results of Apollo, SP-368. NASA Spec. Rep, Washington, DC, pp 43–81
Hengge-Aronis R (2000) The general stress response in Escherichia coli. In: Storz G, Hengge-Aronis R (eds) Bacterial stress responses. ASM Press, Washington, DC
Hiebel TL, Volz PA (1977) Foreign body reactions induced by fungi irradiated in space. Phytologia 35:365–372
Horneck G, Klaus DM, Mancinelli RL (2010) Space microbiology. Microbial Mol Biol Rev 74(1):121–156
Johanson K, Allen PL, Lewis F, Cubano LA, Hyman LE, Hammond TG (2002) Saccharomyces cerevisiae gene expression changes during rotating wall vessel suspension culture. J Appl Physiol 93:2171–2180
Juergensmeyer MA, Juergensmeyer EA, Guikema JA (1999) Long-term exposure to spaceflight conditions affects bacterial response to antibiotics. Microgravity Sci Technol 12(1):41–47
Kacena MA, Todd P (1999) Gentamicin: effect on E. coli in space. Microgravity Sci Technol 12:135–137
Kim HW, Rhee MS (2016) Influence of low-shear modeled microgravity on heat resistance, membrane fatty acid composition, and heat stress-related gene expression in Escherichia coli O157:H7 ATCC 35150, ATCC 43889, ATCC 43890, and ATCC 43895. Appl Environ Microbiol 82(10):2893–2901
Kim W, Tengra FK, Shong J, Marchand N, Chan HK et al (2013a) Effect of spaceflight on Pseudomonas aeruginosa final cell density is modulated by nutrient and oxygen availability. BMC Microbiol 13:241
Kim W, Tengra FK, Young Z, Shong J, Marchand N et al (2013b) Spaceflight promotes biofilm formation by Pseudomonas aeruginosa. PLoS One 8(4):e62437
Kim HW, Matin A, Rhee MS (2014) Microgravity alters the physiological characteristics of Escherichia coli O157:H7 ATCC 35150, ATCC 43889, and ATCC 43895 under different nutrient conditions. Appl Environ Microbiol 80(7):2270–2278
Klaus DM (2001) Clinostats and bioreactors. Gravit Space Biol Bull 14:55–64
Klaus DM, Howard HN (2006) Antibiotic efficacy and microbial virulence during space flight. Trends Biotechnol 24:131–136
Lam J (1980) Production of mucoid microcolonies by Pseudomonas aeruginosa within the infected lungs in cystic fibrosis. Infect Immun 28:546–556
Learn DB, Brestel EP, Seetharama S (1987) Hypochlorite scavenging by Pseudomonas aeruginosa alginate. Infect Immun 55:1813–1818
Li Y, Wang S, Scarpellini G, Gunn B, Xin W et al (2009) Evaluation of new generation Salmonella enterica serovar Typhimurium vaccines with regulated delayed attenuation to induce immune responses against PspA. Proc Natl Acad Sci U S A 106(2):593–598
Lynch SV, Brodie EL, Matin A (2004) Role and regulation of sigma S in general resistance conferred by low-shear simulated microgravity in Escherichia coli. J Bacteriol 186:8207–8212
Lynch SV, Mukundakrishnan K, Benoit MR, Ayyaswamy PS, Matin A (2006) Escherichia coli biofilms formed under low-shear modeled microgravity in a ground-based system. Appl Environ Microbiol 72:7701–7710
Majdalani N, Vanderpool CK, Gottesman S (2005) Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 40:93–113
McClure CD, Schiller NL (1996) Inhibition of macrophage phagocytosis by Pseudomonas aeruginosa rhamnolipids in vitro and in vivo. Curr Microbiol 33:109–117
McLean RJ, Cassanto JM, Barnes MB, Koo JH (2001) Bacterial biofilm formation under microgravity conditions. FEMS Microbiol Lett 195(2):115–119
Nauman EA, Ott CM, Sander E, Tucker DL, Pierson D, Wilson JW et al (2007) Novel quantitative biosystem for modeling physiological fluid shear stress on cells. Appl Environ Microbiol 73:699–705
Nickerson CA, Ott CM, Mister SJ, Morrow BJ, Burns-Keliher L, Pierson DL (2000) Microgravity as a novel environmental signal affecting Salmonella enterica serovar Typhimurium virulence. Infect Immun 68:3147–3152
Nickerson CA, Ott CM, Wilson JW, Ramamurthy R, Pierson DL (2004) Microbial responses to microgravity and other low-shear environments. Microbiol Mol Biol Rev 68:345–361
Orsini SS, Lewis AM, Rice KC (2017) Investigation of simulated microgravity effects on Streptococcus mutans physiology and global gene expression. NPJ Microgravity 3:4
Ott CM (2004) Human immune function and microbial pathogenesis in human spaceflight. Paper presented at the 10th International Symposium on Microbial Ecology, Cancun, Mexico
Pacello F, Rotilio G, Battistoni A (2012) Low-shear modeled microgravity enhances Salmonella enterica resistance to hydrogen peroxide through a mechanism involving KatG and KatN. Open Microbiol J 6:53–64
Pamp SJ, Tolker-Nielsen T (2007) Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J Bacteriol 189:2531–2539
Pfeiffer V, Sittka A, Tomer R, Tedin K, Brinkmann V, Vogel J (2007) A small non-coding RNA of the invasion gene island (SPI-1) represses outer membrane protein synthesis from the Salmonella core genome. Mol Microbiol 66:1174–1191
Pier GB, Coleman F, Grout M, Franklin M, Ohman DE (2001) Role of alginate O acetylation in resistance of mucoid Pseudomonas aeruginosa to opsonic phagocytosis. Infect Immun 69:1895–1901
Pierson DL, Chidambaram M, Heath JD, Mallary L, Mishra SK, Sharma B et al (1996) Epidemiology of Staphylococcus aureus during space flight. FEMS Immunol Med Microbiol 16:273–281
Pierson DL, Mehta SK, Stowe RP (2007) Reactivation of latent herpes viruses in astronauts. In: Ader R (ed) Psychoneuroimmunology. Academic, San Diego, pp 851–868
Purevdorj-Gage B, Sheehan KB, Hyman LE (2006) Effects of low-shear modeled microgravity on cell function, gene expression, and phenotype in Saccharomyces cerevisiae. Appl Environ Microbiol 72:4569–4575
Rosado H, Doyle M, Hinds J, Taylor PW (2010) Low-shear modelled microgravity alters expression of virulence determinants of Staphylococcus aureus. Acta Astronaut 66:408–413
Roy R, Shilpa PP, Bagh S (2016) A systems biology analysis unfolds the molecular pathways and networks of two proteobacteria in spaceflight and simulated microgravity conditions. Astrobiology 16(9):677–689
Sarker S, Ott CM, Barrila J, Nickerson CA (2010) Discovery of spaceflight regulated virulence mechanisms in Salmonella and other microbial pathogens: novel approaches to commercial vaccine development. Gravit Space Biol 23(2):75–78
Sheehan KB, McInnerney K, Purevdorj-Gage B, Altenburg SD, Hyman LE (2007) Yeast genomic expression patterns in response to low-shear modeled microgravity. BMC Genomics 8:3
Shi H, Santander J, Brenneman KE, Wanda SY, Wang S et al (2010a) Live recombinant Salmonella Typhi vaccines constructed to investigate the role of rpoS in eliciting immunity to a heterologous antigen. PLoS One 5(6):e11142
Shi H, Wang S, Roland KL, Gunn BM, Curtiss R III (2010b) Immunogenicity of a live recombinant Salmonella enterica serovar typhimurium vaccine expressing pspA in neonates and infant mice born from naive and immunized mothers. Clin Vaccine Immunol 17(3):363–371
Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ, Greenberg EP (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762–764
Sittka A, Pfeiffer V, Tedin K, Vogel J (2007) The RNA chaperone Hfq is essential for the virulence of Salmonella Typhimurium. Mol Microbiol 63:193–217
Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT et al (2008) Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 4:e1000163
Sommer MOA, Munck C, Toft-Kehler RV, Andersson DI (2017) Prediction of antibiotic resistance: time for a new preclinical paradigm? Nat Rev Microbiol 15(11):689–696. https://doi.org/10.1038/nrmicro.2017
Soni A, O’Sullivan L, Quick LN, Ott CM, Nickerson CA, Wilson JW (2014) Conservation of the low-shear modeled microgravity response in Enterobacteriaceae and analysis of the trp genes in this response. Open Microbiol J 13:51–58
Sriramulu DD, Lunsdorf H, Lam JS, Römling U (2005) Microcolony formation: a novel biofilm model of Pseudomonas aeruginosa for the cystic fibrosis lung. J Med Microbiol 54:667–676
Taylor GR (1974) Recovery of medically important microorganisms from Apollo astronauts. Aerosp Med 45:824–828
Tirumalai MR, Karouia F, Tran Q, Stepanov VG, Bruce RJ et al (2017) The adaptation of Escherichia coli cells grown in simulated microgravity for an extended period is both phenotypic and genomic. NPJ Microgravity 3:15
Tixador R, Richoilley G, Gasset G, Templier J, Bes JC, Moatti N et al (1985) Study of minimal inhibitory concentration of antibiotics on bacteria cultivated in vitro in space (Cytos 2 experiment). Aviat Space Environ Med 56:748–751
Tucker DL, Ott CM, Huff S, Fofanov Y, Pierson DL et al (2007) Characterization of Escherichia coli MG1655 grown in a low-shear modeled microgravity environment. BMC Microbiol 7:15
Volz PA (1990) Mycology studies in space. Mycopathologia 109:89–98
Wagner VE, Iglewski BH (2008) P. aeruginosa biofilms in CF infection. Clin Rev Allergy Immunol 35:124–134
Wang H, Yan Y, Rong D, Wang J, Wang H et al (2016) Increased biofilm formation ability in Klebsiella pneumoniae after short-term exposure to a simulated microgravity environment. Microbiology Open 5(5):793–801
Wilson JW, Ramamurthy R, Porwollik S, McClelland M, Hammond T, Allen P et al (2002a) Microarray analysis identifies Salmonella genes belonging to the low-shear modeled microgravity regulon. Proc Natl Acad Sci U S A 99:13807–13812
Wilson JW, Ott CM, Ramamurthy R, Porwollik S, McClelland M, Pierson DL et al (2002b) Low-Shear modeled microgravity alters the Salmonella enterica serovar Typhimurium stress response in an RpoS-independent manner. Appl Environ Microbiol 68:5408–5416
Wilson JW, Ott CM, Zu Bentrup KH, Ramamurthy R, Quick L, Porwollik S et al (2007) Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq. Proc Natl Acad Sci U S A 104:16299–16304
Wilson JW, Ott CM, Quick L, Davis R, zu Bentrup KH, Crabbé A et al (2008) Media ion composition controls regulatory and virulence response of Salmonella in spaceflight. PLoS One 3:e3923
Xu B, Li C, Zheng Y, Si S, Shi Y (2015) Simulated microgravity affects ciprofloxacin susceptibility and expression of acrAB-tolC genes in E. coli ATCC25922. J Clin Exp Pathol 8(7):7945–7952
Yang J, Barrila J, Roland KL, Ott CM, Nickerson CA (2016) Physiological fluid shear alters the virulence potential of invasive multidrug-resistant non-typhoidal Salmonella typhimurium D23580. NPJ Microgravity 2:16021
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Ott, C.M., Crabbé, A., Wilson, J.W., Barrila, J., Castro-Wallace, S.L., Nickerson, C.A. (2020). Microbial Stress: Spaceflight-Induced Alterations in Microbial Virulence and Infectious Disease Risks for the Crew. In: Choukèr, A. (eds) Stress Challenges and Immunity in Space. Springer, Cham. https://doi.org/10.1007/978-3-030-16996-1_18
Download citation
DOI: https://doi.org/10.1007/978-3-030-16996-1_18
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-16995-4
Online ISBN: 978-3-030-16996-1
eBook Packages: MedicineMedicine (R0)