Skip to main content

Microbiome and Immunity: A Critical Link for Long-Duration Space Exploration Missions

  • Chapter
  • First Online:
Stress Challenges and Immunity in Space
  • 1303 Accesses

Abstract

The human microbiome is the collection of trillions of microorganisms that live in and on the human body. It is mostly composed of bacteria, viruses, archaea, and unicellular eukaryotes that have coevolved with us over millions of years. The microbiome is essential to human health, being involved in the processing and absorption of complex nutrients, the synthesis of vitamins and antioxidants, the maturation and modulation of the immune system and the prevention of infections by pathogenic organisms. Therefore, qualitative or quantitative shifts in the gut microbiota, commonly known as dysbiosis, as a consequence of host pathobiology, alterations of diet, medications, and other environmental triggers, can perturb critical inter-microbe as well as host–microbe relationships to initiate pathophysiological processes leading to human disease. To maintain health, the immune system plays an essential role in maintaining a delicate balance between eliminating invading pathogens and keeping the homeostatic relationship with beneficial resident microorganisms of the gastrointestinal tract. At the same time, resident bacteria have a significant immunomodulatory activity that profoundly shape mammalian immunity. During a mission to space, astronauts are exposed to a number of stressors (microgravity, sleep deprivation, radiation, dietary changes, etc.) that are likely to affect the composition and dynamic of the astronauts’ microbiome. Several studies on specific culturable commensal and opportunistic pathogenic bacteria performed under real or simulated microgravity conditions suggest that space travel can affect the composition and function of the microbiome, including bacterial virulence, antibiotic resistance, and growth. This chapter will focus on what is currently known about the interaction between the human intestinal microbiota and the immune response and how conditions found in space might alter this interaction and pose a risk to astronauts’ health.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Acharya N, Penukonda S, Shcheglova T, Hagymasi AT, Basu S, Srivastava PK (2017) Endocannabinoid system acts as a regulator of immune homeostasis in the gut. Proc Natl Acad Sci U S A 114:5005–5010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahern PP, Schiering C, Buonocore S, McGeachy MJ, Cua DJ, Maloy KJ, Powrie F (2010) Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity 33:279–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allebban Z, Ichiki AT, Gibson LA, Jones JB, Congdon CC, Lange RD (1994) Effects of spaceflight on the number of rat peripheral blood leukocytes and lymphocyte subsets. J Leukoc Biol 55:209–213

    Article  CAS  PubMed  Google Scholar 

  • Allen CA, Niesel DW, Torres AG (2008) The effects of low-shear stress on Adherent-invasive Escherichia coli. Environ Microbiol 10:1512–1525

    Article  CAS  PubMed  Google Scholar 

  • Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, Rudensky AY (2013) Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504:451–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H, Khan MT, Zhang J, Li J, Xiao L, Al-Aama J, Zhang D, Lee YS, Kotowska D, Colding C, Tremaroli V, Yin Y, Bergman S, Xu X, Madsen L, Kristiansen K, Dahlgren J, Wang J (2015) Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17:852

    Article  CAS  PubMed  Google Scholar 

  • Bailey MT (2014) Influence of stressor-induced nervous system activation on the intestinal microbiota and the importance for immunomodulation. Adv Exp Med Biol 817:255–276

    Article  CAS  PubMed  Google Scholar 

  • Bailey MT, Engler H, Sheridan JF (2006) Stress induces the translocation of cutaneous and gastrointestinal microflora to secondary lymphoid organs of C57BL/6 mice. J Neuroimmunol 171:29–37

    Article  CAS  PubMed  Google Scholar 

  • Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M (2011) Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun 25:397–407

    Article  CAS  PubMed  Google Scholar 

  • Batkai L, Varkonyi A, Minarovits J (1999) The effect of simulated microgravity conditions on the TNF-alpha production by human PBMCS. J Gravit Physiol 6:P109–P110

    CAS  PubMed  Google Scholar 

  • Benoit MR, Li W, Stodieck LS, Lam KS, Winther CL, Roane TM, Klaus DM (2006) Microbial antibiotic production aboard the International Space Station. Appl Microbiol Biotechnol 70:403–411

    Article  CAS  PubMed  Google Scholar 

  • Brandl K, Plitas G, Schnabl B, DeMatteo RP, Pamer EG (2007) MyD88-mediated signals induce the bactericidal lectin RegIII gamma and protect mice against intestinal Listeria monocytogenes infection. J Exp Med 204:1891–1900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown LR, Fromme WJ, Handler SF, Wheatcroft MG, Johnston DA (1976) Effect of Skylab missions on clinical and microbiologic aspects of oral health. J Am Dent Assoc 93:357–363

    Article  CAS  PubMed  Google Scholar 

  • Cameron DJ (1985) Specificity of macrophage-mediated cytotoxicity: role of target and effector cell fucose. Immunol Lett 11:39–44

    Article  CAS  PubMed  Google Scholar 

  • Cani PD, Plovier H, Van Hul M, Geurts L, Delzenne NM, Druart C, Everard A (2016) Endocannabinoids--at the crossroads between the gut microbiota and host metabolism. Nat Rev Endocrinol 12:133–143

    Article  CAS  PubMed  Google Scholar 

  • Castro SL, Nelman-Gonzalez M, Nickerson CA, Ott CM (2011) Induction of attachment-independent biofilm formation and repression of Hfq expression by low-fluid-shear culture of Staphylococcus aureus. Appl Environ Microbiol 77:6368–6378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castro-Wallace S, Stahl S, Voorhies A, Lorenzi H, Douglas GL (2017) Response of Lactobacillus acidophilus ATCC 4356 to low-shear modeled microgravity. Acta Astronaut 139:463–468

    Article  Google Scholar 

  • Chapes SK, Morrison DR, Guikema JA, Lewis ML, Spooner BS (1992) Cytokine secretion by immune cells in space. J Leukoc Biol 52:104–110

    Article  CAS  PubMed  Google Scholar 

  • Ciferri O, Tiboni O, Di Pasquale G, Orlandoni AM, Marchesi ML (1986) Effects of microgravity on genetic recombination in Escherichia coli. Naturwissenschaften 73:418–421

    Article  CAS  PubMed  Google Scholar 

  • Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN (2010) Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med 16:228–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coghill JM, Sarantopoulos S, Moran TP, Murphy WJ, Blazar BR, Serody JS (2011) Effector CD4+ T cells, the cytokines they generate, and GVHD: something old and something new. Blood 117:3268–3276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cogoli A (1993) The effect of space flight on human cellular immunity. Environ Med 37:107–116

    CAS  PubMed  Google Scholar 

  • Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R (2009) Bacterial community variation in human body habitats across space and time. Science 326:1694–1697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crabbe A, Pycke B, Van Houdt R, Monsieurs P, Nickerson C, Leys N, Cornelis P (2010) Response of Pseudomonas aeruginosa PAO1 to low shear modelled microgravity involves AlgU regulation. Environ Microbiol 12:1545–1564

    CAS  PubMed  Google Scholar 

  • Crabbe A, Schurr MJ, Monsieurs P, Morici L, Schurr J, Wilson JW, Ott CM, Tsaprailis G, Pierson DL, Stefanyshyn-Piper H, Nickerson CA (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

    Article  CAS  PubMed  Google Scholar 

  • Crucian B, Sams C (2009) HRP evidence report: risk of crew adverse health event due to altered immune response. HRP evidence report. NASA, Washington, DC

    Google Scholar 

  • Crucian BE, Zwart SR, Mehta S, Uchakin P, Quiriarte HD, Pierson D, Sams CF, Smith SM (2014a) Plasma cytokine concentrations indicate that in vivo hormonal regulation of immunity is altered during long-duration spaceflight. J Interferon Cytokine Res 34:778–786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crucian B, Simpson RJ, Mehta S, Stowe R, Chouker A, Hwang SA, Actor JK, Salam AP, Pierson D, Sams C (2014b) Terrestrial stress analogs for spaceflight associated immune system dysregulation. Brain Behav Immun 39:23–32

    Article  CAS  PubMed  Google Scholar 

  • Crucian B, Stowe RP, Mehta S, Quiriarte H, Pierson D, Sams C (2015) Alterations in adaptive immunity persist during long-duration spaceflight. NPJ Microgravity 1:15013

    Article  PubMed  PubMed Central  Google Scholar 

  • Crucian B, Johnston S, Mehta S, Stowe R, Uchakin P, Quiriarte H, Pierson D, Laudenslager ML, Sams C (2016) A case of persistent skin rash and rhinitis with immune system dysregulation onboard the International Space Station. J Allergy Clin Immunol Pract 4:759–762e8

    Article  PubMed  Google Scholar 

  • Crucian BE, Chouker A, Simpson RJ, Mehta S, Marshall G, Smith SM, Zwart SR, Heer M, Ponomarev S, Whitmire A, Frippiat JP, Douglas GL, Lorenzi H, Buchheim JI, Makedonas G, Ginsburg GS, Ott CM, Pierson DL, Krieger SS, Baecker N, Sams C (2018) Immune system dysregulation during spaceflight: potential countermeasures for deep space exploration missions. Front Immunol 9:1437

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Palma G, Blennerhassett P, Lu J, Deng Y, Park AJ, Green W, Denou E, Silva MA, Santacruz A, Sanz Y, Surette MG, Verdu EF, Collins SM, Bercik P (2015) Microbiota and host determinants of behavioural phenotype in maternally separated mice. Nat Commun 6:7735

    Article  PubMed  CAS  Google Scholar 

  • Decelle JG, Taylor GR (1976) Autoflora in the upper respiratory tract of Apollo astronauts. Appl Environ Microbiol 32:659–665

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elinav E, Strowig T, Kau AL, Henao-Mejia J, Thaiss CA, Booth CJ, Peaper DR, Bertin J, Eisenbarth SC, Gordon JI, Flavell RA (2011) NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 145:745–757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eriguchi Y, Nakamura K, Hashimoto D, Shimoda S, Shimono N, Akashi K, Ayabe T, Teshima T (2015) Decreased secretion of Paneth cell alpha-defensins in graft-versus-host disease. Transpl Infect Dis 17:702–706

    Article  CAS  PubMed  Google Scholar 

  • Feuerecker M, Crucian BE, Quintens R, Buchheim JI, Salam AP, Rybka A, Moreels M, Strewe C, Stowe R, Mehta S, Schelling G, Thiel M, Baatout S, Sams C, Chouker A (2019) Immune sensitization during one year in the Antarctic high altitude Concordia Environment. Allergy 74:64. https://doi.org/10.1111/all.13545

    Article  CAS  PubMed  Google Scholar 

  • Foster JS, Khodadad CL, Ahrendt SR, Parrish ML (2013) Impact of simulated microgravity on the normal developmental time line of an animal-bacteria symbiosis. Sci Rep 3:1340

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, Takahashi M, Fukuda NN, Murakami S, Miyauchi E, Hino S, Atarashi K, Onawa S, Fujimura Y, Lockett T, Clarke JM, Topping DL, Tomita M, Hori S, Ohara O, Morita T, Koseki H, Kikuchi J, Honda K, Hase K, Ohno H (2013) Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504:446–450

    Article  CAS  PubMed  Google Scholar 

  • Ganji-Arjenaki M, Rafieian-Kopaei M (2018) Probiotics are a good choice in remission of inflammatory bowel diseases: a meta analysis and systematic review. J Cell Physiol 233:2091–2103

    Article  CAS  PubMed  Google Scholar 

  • Gebbers JO, Laissue JA (1989) Immunologic structures and functions of the gut. Schweiz Arch Tierheilkd 131:221–238

    CAS  PubMed  Google Scholar 

  • Gibson GR, Wang X (1994) Regulatory effects of bifidobacteria on the growth of other colonic bacteria. J Appl Bacteriol 77:412–420

    Article  CAS  PubMed  Google Scholar 

  • Gmunder FK, Konstantinova I, Cogoli A, Lesnyak A, Bogomolov W, Grachov AW (1994) Cellular immunity in cosmonauts during long duration spaceflight on board the orbital MIR station. Aviat Space Environ Med 65:419–423

    CAS  PubMed  Google Scholar 

  • Gomez del Pulgar T, Benitah SA, Valeron PF, Espina C, Lacal JC (2005) Rho GTPase expression in tumourigenesis: evidence for a significant link. Bioessays 27:602–613

    Article  PubMed  CAS  Google Scholar 

  • Goncharova GI, Liz’ko NN, Liannaia AM, Shilov VM, Spitsa TI (1981) Bifidobacterium flora status of cosmonauts before and after completing space flights. Kosm Biol Aviakosm Med 15:14–18

    CAS  PubMed  Google Scholar 

  • Hales NW, Yamauchi K, Alicea A, Sundaresan A, Pellis NR, Kulkarni AD (2002) A countermeasure to ameliorate immune dysfunction in in vitro simulated microgravity environment: role of cellularnucleotide nutrition. In Vitro Cell Dev Biol Anim 38:213–217

    Article  CAS  PubMed  Google Scholar 

  • Hammond TG, Stodieck L, Birdsall HH, Becker JL, Koenig P, Hammond JS, Gunter MA, Allen PL (2013) Effects of microgravity on the virulence of Listeria monocytogenes, Enterococcus faecalis, Candida albicans, and methicillin-resistant Staphylococcus aureus. Astrobiology 13:1081–1090

    Article  CAS  PubMed  Google Scholar 

  • Hayase E, Hashimoto D, Nakamura K, Noizat C, Ogasawara R, Takahashi S, Ohigashi H, Yokoi Y, Sugimoto R, Matsuoka S, Ara T, Yokoyama E, Yamakawa T, Ebata K, Kondo T, Hiramine R, Aizawa T, Ogura Y, Hayashi T, Mori H, Kurokawa K, Tomizuka K, Ayabe T, Teshima T (2017) R-Spondin1 expands Paneth cells and prevents dysbiosis induced by graft-versus-host disease. J Exp Med 214:3507–3518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ichiki AT, Gibson LA, Jago TL, Strickland KM, Johnson DL, Lange RD, Allebban Z (1996) Effects of spaceflight on rat peripheral blood leukocytes and bone marrow progenitor cells. J Leukoc Biol 60:37–43

    Article  CAS  PubMed  Google Scholar 

  • Ilyin VK (2005) Microbiological status of cosmonauts during orbital spaceflights on Salyut and Mir orbital stations. Acta Astronaut 56:839–850

    Article  CAS  PubMed  Google Scholar 

  • Inohara N, Ogura Y, Fontalba A, Gutierrez O, Pons F, Crespo J, Fukase K, Inamura S, Kusumoto S, Hashimoto M, Foster SJ, Moran AP, Fernandez-Luna JL, Nunez G (2003) Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn’s disease. J Biol Chem 278:5509–5512

    Article  CAS  PubMed  Google Scholar 

  • Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269

    Article  CAS  PubMed  Google Scholar 

  • Kaur I, Simons ER, Castro VA, Mark Ott C, Pierson DL (2004) Changes in neutrophil functions in astronauts. Brain Behav Immun 18:443–450

    Article  CAS  PubMed  Google Scholar 

  • Kaur I, Simons ER, Castro VA, Ott CM, Pierson DL (2005) Changes in monocyte functions of astronauts. Brain Behav Immun 19:547–554

    Article  CAS  PubMed  Google Scholar 

  • Kelsall B (2008) Recent progress in understanding the phenotype and function of intestinal dendritic cells and macrophages. Mucosal Immunol 1:460–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim W, Tengra FK, Shong J, Marchand N, Chan HK, Young Z, Pangule RC, Parra M, Dordick JS, Plawsky JL, Collins CH (2013a) Effect of spaceflight on Pseudomonas aeruginosa final cell density is modulated by nutrient and oxygen availability. BMC Microbiol 13:241

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim W, Tengra FK, Young Z, Shong J, Marchand N, Chan HK, Pangule RC, Parra M, Dordick JS, Plawsky JL, Collins CH (2013b) Spaceflight promotes biofilm formation by Pseudomonas aeruginosa. PLoS One 8:e62437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klaus DM, Howard HN (2006) Antibiotic efficacy and microbial virulence during space flight. Trends Biotechnol 24:131–136

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, Nunez G, Flavell RA (2005) Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 307:731–734

    Article  CAS  PubMed  Google Scholar 

  • Lawal A, Jejelowo OA, Rosenzweig JA (2010) The effects of low-shear mechanical stress on Yersinia pestis virulence. Astrobiology 10:881–888

    Article  PubMed  Google Scholar 

  • Lawal A, Kirtley ML, van Lier CJ, Erova TE, Kozlova EV, Sha J, Chopra AK, Rosenzweig JA (2013) The effects of modeled microgravity on growth kinetics, antibiotic susceptibility, cold growth, and the virulence potential of a Yersinia pestis ymoA-deficient mutant and its isogenic parental strain. Astrobiology 13:821–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leid JG, Willson CJ, Shirtliff ME, Hassett DJ, Parsek MR, Jeffers AK (2005) The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gamma-mediated macrophage killing. J Immunol 175:7512–7518

    Article  CAS  PubMed  Google Scholar 

  • Lencner AA, Lencner CP, Mikelsaar ME, Tjuri ME, Toom MA, Valjaots ME, Silov VM, Liz’ko NN, Legenkov VI, Reznikov IM (1984) The quantitative composition of the intestinal lactoflora before and after space flights of different lengths. Nahrung 28:607–613

    Article  CAS  PubMed  Google Scholar 

  • Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848

    Article  CAS  PubMed  Google Scholar 

  • Lievin V, Peiffer I, Hudault S, Rochat F, Brassart D, Neeser JR, Servin AL (2000) Bifidobacterium strains from resident infant human gastrointestinal microflora exert antimicrobial activity. Gut 47:646–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lizko NN, Silov VM, Syrych GD (1984) Events in he development of dysbacteriosis of the intestines in man under extreme conditions. Nahrung 28:599–605

    Article  CAS  PubMed  Google Scholar 

  • Louis F, Deroanne C, Nusgens B, Vico L, Guignandon A (2015) RhoGTPases as key players in mammalian cell adaptation to microgravity. Biomed Res Int 2015:747693

    PubMed Central  PubMed  Google Scholar 

  • Macia L, Tan J, Vieira AT, Leach K, Stanley D, Luong S, Maruya M, Ian McKenzie C, Hijikata A, Wong C, Binge L, Thorburn AN, Chevalier N, Ang C, Marino E, Robert R, Offermanns S, Teixeira MM, Moore RJ, Flavell RA, Fagarasan S, Mackay CR (2015) Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat Commun 6:6734

    Article  CAS  PubMed  Google Scholar 

  • Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H, Zinkernagel RM (2000) A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288:2222–2226

    Article  CAS  PubMed  Google Scholar 

  • McLean RJ, Cassanto JM, Barnes MB, Koo JH (2001) Bacterial biofilm formation under microgravity conditions. FEMS Microbiol Lett 195:115–119

    Article  CAS  PubMed  Google Scholar 

  • Mehrpouya-Bahrami P, Chitrala KN, Ganewatta MS, Tang C, Murphy EA, Enos RT, Velazquez KT, McCellan J, Nagarkatti M, Nagarkatti P (2017) Blockade of CB1 cannabinoid receptor alters gut microbiota and attenuates inflammation and diet-induced obesity. Sci Rep 7:15645

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mehta SK, Crucian BE, Stowe RP, Simpson RJ, Ott CM, Sams CF, Pierson DL (2013) Reactivation of latent viruses is associated with increased plasma cytokines in astronauts. Cytokine 61:205–209

    Article  CAS  PubMed  Google Scholar 

  • Mehta SK, Laudenslager ML, Stowe RP, Crucian BE, Sams CF, Pierson DL (2014) Multiple latent viruses reactivate in astronauts during Space Shuttle missions. Brain Behav Immun 41:210–217

    Article  CAS  PubMed  Google Scholar 

  • Muccioli GG, Naslain D, Backhed F, Reigstad CS, Lambert DM, Delzenne NM, Cani PD (2010) The endocannabinoid system links gut microbiota to adipogenesis. Mol Syst Biol 6:392

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogura Y, Lala S, Xin W, Smith E, Dowds TA, Chen FF, Zimmermann E, Tretiakova M, Cho JH, Hart J, Greenson JK, Keshav S, Nunez G (2003) Expression of NOD2 in Paneth cells: a possible link to Crohn’s ileitis. Gut 52:1591–1597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ott CM, Oubre C, Wallace S, Mehta SK, Pierson DL (2016) Risk of adverse health effects due to host-microorganisms interactions. NASA, Human Health Countermeasures (HHC) Element, Washington, DC

    Google Scholar 

  • Ottman N, Smidt H, de Vos WM, Belzer C (2012) The function of our microbiota: who is out there and what do they do? Front Cell Infect Microbiol 2:104

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pachenari M, Seyedpour SM, Janmaleki M, Babazadeh Shayan S, Taranejoo S, Hosseinkhani H (2014) Mechanical properties of cancer cytoskeleton depend on actin filaments to microtubules content: investigating different grades of colon cancer cell lines. J Biomech 47:373–379

    Article  CAS  PubMed  Google Scholar 

  • Paulsen K, Tauber S, Dumrese C, Bradacs G, Simmet DM, Golz N, Hauschild S, Raig C, Engeli S, Gutewort A, Hurlimann E, Biskup J, Unverdorben F, Rieder G, Hofmanner D, Mutschler L, Krammer S, Buttron I, Philpot C, Huge A, Lier H, Barz I, Engelmann F, Layer LE, Thiel CS, Ullrich O (2015) Regulation of ICAM-1 in cells of the monocyte/macrophage system in microgravity. Biomed Res Int 2015:538786

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peterson DA, McNulty NP, Guruge JL, Gordon JI (2007) IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2:328–339

    Article  CAS  PubMed  Google Scholar 

  • Pull SL, Doherty JM, Mills JC, Gordon JI, Stappenbeck TS (2005) Activated macrophages are an adaptive element of the colonic epithelial progenitor niche necessary for regenerative responses to injury. Proc Natl Acad Sci U S A 102:99–104

    Article  CAS  PubMed  Google Scholar 

  • Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118:229–241

    Article  CAS  PubMed  Google Scholar 

  • Rea K, Dinan TG, Cryan JF (2016) The microbiome: a key regulator of stress and neuroinflammation. Neurobiol Stress 4:23–33

    Article  PubMed  PubMed Central  Google Scholar 

  • Ritchie LE, Taddeo SS, Weeks BR, Lima F, Bloomfield SA, Azcarate-Peril MA, Zwart SR, Smith SM, Turner ND (2015) Space environmental factor impacts upon murine colon microbiota and mucosal homeostasis. PLoS One 10:e0125792

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saei AA, Barzegari A (2012) The microbiome: the forgotten organ of the astronaut’s body--probiotics beyond terrestrial limits. Future Microbiol 7:1037–1046

    Article  CAS  PubMed  Google Scholar 

  • Savary CA, Grazziuti ML, Przepiorka D, Tomasovic SP, McIntyre BW, Woodside DG, Pellis NR, Pierson DL, Rex JH (2001) Characteristics of human dendritic cells generated in a microgravity analog culture system. In Vitro Cell Dev Biol Anim 37:216–222

    Article  CAS  PubMed  Google Scholar 

  • Sender R, Fuchs S, Milo R (2016) Revised estimates for the number of human and bacteria cells in the body. PLoS Biol 14:e1002533

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shao D, Yao L, Riaz MS, Zhu J, Shi J, Jin M, Huang Q, Yang H (2017) Simulated microgravity affects some biological characteristics of Lactobacillus acidophilus. Appl Microbiol Biotechnol 101:3439–3449

    Article  CAS  PubMed  Google Scholar 

  • Shen Y, Giardino Torchia ML, Lawson GW, Karp CL, Ashwell JD, Mazmanian SK (2012) Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 12:509–520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, Glickman JN, Garrett WS (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341:569–573

    Article  CAS  PubMed  Google Scholar 

  • Sonnenberg GF, Monticelli LA, Alenghat T, Fung TC, Hutnick NA, Kunisawa J, Shibata N, Grunberg S, Sinha R, Zahm AM, Tardif MR, Sathaliyawala T, Kubota M, Farber DL, Collman RG, Shaked A, Fouser LA, Weiner DB, Tessier PA, Friedman JR, Kiyono H, Bushman FD, Chang KM, Artis D (2012) Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 336:1321–1325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stowe RP, Sams CF, Mehta SK, Kaur I, Jones ML, Feeback DL, Pierson DL (1999) Leukocyte subsets and neutrophil function after short-term spaceflight. J Leukoc Biol 65:179–186

    Article  CAS  PubMed  Google Scholar 

  • Strewe C, Feuerecker M, Nichiporuk I, Kaufmann I, Hauer D, Morukov B, Schelling G, Chouker A (2012) Effects of parabolic flight and spaceflight on the endocannabinoid system in humans. Rev Neurosci 23:673–680

    Article  CAS  PubMed  Google Scholar 

  • Tauber S, Lauber BA, Paulsen K, Layer LE, Lehmann M, Hauschild S, Shepherd NR, Polzer J, Segerer J, Thiel CS, Ullrich O (2017) Cytoskeletal stability and metabolic alterations in primary human macrophages in long-term microgravity. PLoS One 12:e0175599

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Taylor GR, Janney RP (1992) In vivo testing confirms a blunting of the human cell-mediated immune mechanism during space flight. J Leukoc Biol 51:129–132

    Article  CAS  PubMed  Google Scholar 

  • Taylor PW, Sommer AP (2005) Towards rational treatment of bacterial infections during extended space travel. Int J Antimicrob Agents 26:183–187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turek FW, Vitaterna MH, Jiang P, Keshavarzian A, Green SJ (2017) Metagenomic sequencing of the bacteriome in GI tract of twin astronauts on ground and on one-year ISS mission. In: Space life & physical sciences research & applications division task book. https://taskbook.nasaprs.com/Publication/index.cfm?action=public_query_taskbook_content&TASKID=11124

    Google Scholar 

  • Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV (2008) Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci U S A 105:20858–20863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vega FM, Ridley AJ (2008) Rho GTPases in cancer cell biology. FEBS Lett 582:2093–2101

    Article  CAS  PubMed  Google Scholar 

  • Voorhies AA, Mehta SK, Crucian BE, Torralba M, Moncera K, Feiveson A, Zurek-Varela EE, Pierson DL, Ott CM, Lorenzi HA (2017) Study of the impact of long-term space travel on the astronaut’s microbiome. In: Space life & physical sciences research & applications division task book. https://taskbook.nasaprs.com/Publication/index.cfm?action=public_query_taskbook_content&TASKID=11370

    Google Scholar 

  • Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, Petras RE, Shen B, Schaeffeler E, Schwab M, Linzmeier R, Feathers RW, Chu H, Lima H Jr, Fellermann K, Ganz T, Stange EF, Bevins CL (2005) Reduced Paneth cell alpha-defensins in ileal Crohn’s disease. Proc Natl Acad Sci U S A 102:18129–18134

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A 95:6578–6583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson JW, Ott CM, Honer zu Bentrup K, Ramamurthy R, Quick L, Porwollik S, Cheng P, McClelland M, Tsaprailis G, Radabaugh T, Hunt A, Fernandez D, Richter E, Shah M, Kilcoyne M, Joshi L, Nelman-Gonzalez M, Hing S, Parra M, Dumars P, Norwood K, Bober R, Devich J, Ruggles A, Goulart C, Rupert M, Stodieck L, Stafford P, Catella L, Schurr MJ, Buchanan K, Morici L, McCracken J, Allen P, Baker-Coleman C, Hammond T, Vogel J, Nelson R, Pierson DL, Stefanyshyn-Piper HM, Nickerson CA (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson JW, Ott CM, Quick L, Davis R, Honer zu Bentrup K, Crabbe A, Richter E, Sarker S, Barrila J, Porwollik S, Cheng P, McClelland M, Tsaprailis G, Radabaugh T, Hunt A, Shah M, Nelman-Gonzalez M, Hing S, Parra M, Dumars P, Norwood K, Bober R, Devich J, Ruggles A, CdeBaca A, Narayan S, Benjamin J, Goulart C, Rupert M, Catella L, Schurr MJ, Buchanan K, Morici L, McCracken J, Porter MD, Pierson DL, Smith SM, Mergeay M, Leys N, Stefanyshyn-Piper HM, Gorie D, Nickerson CA (2008) Media ion composition controls regulatory and virulence response of Salmonella in spaceflight. PLoS One 3:e3923

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamaguchi H, Condeelis J (2007) Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim Biophys Acta 1773:642–652

    Article  CAS  PubMed  Google Scholar 

  • Yi B, Rykova M, Jager G, Feuerecker M, Horl M, Matzel S, Ponomarev S, Vassilieva G, Nichiporuk I, Chouker A (2015) Influences of large sets of environmental exposures on immune responses in healthy adult men. Sci Rep 5:13367

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zea L, Prasad N, Levy SE, Stodieck L, Jones A, Shrestha S, Klaus D (2016) A molecular genetic basis explaining altered bacterial behavior in space. PLoS One 11:e0164359

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zea L, Larsen M, Estante F, Qvortrup K, Moeller R, Dias de Oliveira S, Stodieck L, Klaus D (2017) Phenotypic changes exhibited by E. coli cultured in space. Front Microbiol 8:1598

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hernan Lorenzi .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Lorenzi, H. (2020). Microbiome and Immunity: A Critical Link for Long-Duration Space Exploration Missions. In: Choukèr, A. (eds) Stress Challenges and Immunity in Space. Springer, Cham. https://doi.org/10.1007/978-3-030-16996-1_34

Download citation

  • DOI: https://doi.org/10.1007/978-3-030-16996-1_34

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-030-16995-4

  • Online ISBN: 978-3-030-16996-1

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics