3,750
Views
24
CrossRef citations to date
0
Altmetric
Research Paper/Report

Effects of spaceflight on the composition and function of the human gut microbiota

ORCID Icon, , , , , , , , , , , , , , , , , , & show all
Pages 807-819 | Received 23 Jul 2019, Accepted 18 Dec 2019, Published online: 10 Jan 2020

References

  • Deng Z, Mu J, Tseng M, Wattenberg B, Zhuang X, Egilmez NK, Wang Q, Zhang L, Norris J, Guo H, et al. Enterobacteria-secreted particles induce production of exosome-like S1P-containing particles by intestinal epithelium to drive Th17-mediated tumorigenesis. Nat Commun. 2015;6:6956. doi:10.1038/ncomms7956.
  • Gensollen T, Iyer SS, Kasper DL, Blumberg RS. How colonization by microbiota in early life shapes the immune system. Science. 2016;352(6285):539–544. doi:10.1126/science.aad9378.
  • Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, et al. Enterotypes of the human gut microbiome. Nature. 2011;473(7346):174–180. doi:10.1038/nature09944.
  • Spanogiannopoulos P, Bess EN, Carmody RN, Turnbaugh PJ. The microbial pharmacists within us: a metagenomic view of xenobiotic metabolism. Nat Rev Microbiol. 2016;14(5):273–287. doi:10.1038/nrmicro.2016.17.
  • Schroeder BO, Backhed F. Signals from the gut microbiota to distant organs in physiology and disease. Nat Med. 2016;22(10):1079–1089. doi:10.1038/nm.4185.
  • Walter J, Ley R. The human gut microbiome: ecology and recent evolutionary changes. Annu Rev Microbiol. 2011;65:411–429. doi:10.1146/annurev-micro-090110-102830.
  • Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016;165(6):1332–1345. doi:10.1016/j.cell.2016.05.041.
  • Degnan PH, Taga ME, Goodman AL. Vitamin B12 as a modulator of gut microbial ecology. Cell Metab. 2014;20(5):769–778. doi:10.1016/j.cmet.2014.10.002.
  • Macpherson AJ, de Aguero MG, Ganal-Vonarburg SC. How nutrition and the maternal microbiota shape the neonatal immune system. Nat Rev Immunol. 2017;17(8):508–517. doi:10.1038/nri.2017.58.
  • Planer JD, Peng Y, Kau AL, Blanton LV, Ndao IM, Tarr PI, Warner BB, Gordon JI. Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice. Nature. 2016;534(7606):263–266. doi:10.1038/nature17940.
  • Candela M, Biagi E, Turroni S, Maccaferri S, Figini P, Brigidi P. Dynamic efficiency of the human intestinal microbiota. Crit Rev Microbiol. 2015;41(2):165–171. doi:10.3109/1040841X.2013.813900.
  • Flores GE, Caporaso JG, Henley JB, Rideout JR, Domogala D, Chase J, Leff JW, Vazquez-Baeza Y, Gonzalez A, Knight R, et al. Temporal variability is a personalized feature of the human microbiome. Genome Biol. 2014;15(12):531. doi:10.1186/s13059-014-0531-y.
  • Lax S, Smith DP, Hampton-Marcell J, Owens SM, Handley KM, Scott NM, Gibbons SM, Larsen P, Shogan BD, Weiss S, et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science. 2014;345(6200):1048–1052. doi:10.1126/science.1254529.
  • Song SJ, Lauber C, Costello EK, Lozupone CA, Humphrey G, Berg-Lyons D, Caporaso JG, Knights D, Clemente JC, Nakielny S, et al. Cohabiting family members share microbiota with one another and with their dogs. eLife. 2013;2:e00458. doi:10.7554/eLife.00458.
  • Hao Z, Wang W, Guo R, Liu H. Faecalibacterium prausnitzii (ATCC 27766) has preventive and therapeutic effects on chronic unpredictable mild stress-induced depression-like and anxiety-like behavior in rats. Psychoneuroendocrinology. 2019;104:132–142. doi:10.1016/j.psyneuen.2019.02.025.
  • Li L, Su Q, Xie B, Duan L, Zhao W, Hu D, Wu R, Liu H. Gut microbes in correlation with mood: case study in a closed experimental human life support system. Neurogastroenterol Motil. 2016;28(8):1233–1240. doi:10.1111/nmo.2016.28.issue-8.
  • Turroni S, Rampelli S, Biagi E, Consolandi C, Severgnini M, Peano C, Quercia S, Soverini M, Carbonero FG, Bianconi G, et al. Temporal dynamics of the gut microbiota in people sharing a confined environment, a 520-day ground-based space simulation, MARS500. Microbiome. 2017;5(1):39. doi:10.1186/s40168-017-0256-8.
  • Chapes SK. Lessons from Immune 1-3: what did we learn and what do we need to do in the future? J Gravitational Physiol. 2004;11:P45–48.
  • Zhang LF, Hargens AR. Spaceflight-induced intracranial hypertension and visual impairment: pathophysiology and countermeasures. Physiol Rev. 2018;98(1):59–87. doi:10.1152/physrev.00017.2016.
  • Cogoli A, Cogoli-Greuter M. Activation and proliferation of lymphocytes and other mammalian cells in microgravity. Adv Space Biol Med. 1997;6:33–79.
  • Sonnenfeld G. Extreme environments and the immune system: effects of spaceflight on immune responses. J Allergy Clin Immunol. 2001;107(1):19–20. doi:10.1067/mai.2001.112034.
  • Klaus DM, Howard HN. Antibiotic efficacy and microbial virulence during space flight. Trends Biotechnol. 2006;24(3):131–136. doi:10.1016/j.tibtech.2006.01.008.
  • Mermel LA. Infection prevention and control during prolonged human space travel. Clin Infect Dis. 2013;56(1):123–130. doi:10.1093/cid/cis861.
  • Cohrs RJ, Mehta SK, Schmid DS, Gilden DH, Pierson DL. Asymptomatic reactivation and shed of infectious varicella zoster virus in astronauts. J Med Virol. 2008;80(6):1116–1122. doi:10.1002/(ISSN)1096-9071.
  • Mehta SK, Cohrs RJ, Forghani B, Zerbe G, Gilden DH, Pierson DL. Stress-induced subclinical reactivation of varicella zoster virus in astronauts. J Med Virol. 2004;72(1):174–179. doi:10.1002/(ISSN)1096-9071.
  • Wang H, Yan Y, Rong D, Wang J, Wang H, Liu Z, Wang J, Yang R, Han Y. Increased biofilm formation ability in Klebsiella pneumoniae after short-term exposure to a simulated microgravity environment. MicrobiologyOpen. 2016;5(5):793–801. doi:10.1002/mbo3.2016.5.issue-5.
  • Wilson JW, Ott CM, Honer Zu Bentrup K, Ramamurthy R, Quick L, Porwollik S, Cheng P, McClelland M, Tsaprailis G, Radabaugh T, et al. Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq. Proc Natl Acad Sci USA. 2007;104(41):16299–16304. doi:10.1073/pnas.0707155104.
  • Garrett-Bakelman FE, Darshi M, Green SJ, Gur RC, Lin L, Macias BR, McKenna MJ, Meydan C, Mishra T, Nasrini J, et al. The NASA Twins study: a multidimensional analysis of a year-long human spaceflight. Science. 2019;364(6436). doi:10.1126/science.aav6390.
  • Voorhies AA, Mark Ott C, Mehta S, Pierson DL, Crucian BE, Feiveson A, Oubre CM, Torralba M, Moncera K, Zhang Y, et al. Study of the impact of long-duration space missions at the international space station on the astronaut microbiome. Sci Rep. 2019;9(1):9911. doi:10.1038/s41598-019-46303-8.
  • Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience. 2012;1(1):18. doi:10.1186/2047-217X-1-18.
  • Qin N, Yang F, Li A, Prifti E, Chen Y, Shao L, Guo J, Le Chatelier E, Yao J, Wu L, et al. Alterations of the human gut microbiome in liver cirrhosis. Nature. 2014;513(7516):59–64. doi:10.1038/nature13568.
  • Nielsen HB, Almeida M, Juncker AS, Rasmussen S, Li J, Sunagawa S, Plichta DR, Gautier L, Pedersen AG, Le Chatelier E, et al. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat Biotechnol. 2014;32(8):822–828. doi:10.1038/nbt.2939.
  • Karlsson FH, Tremaroli V, Nookaew I, Bergstrom G, Behre CJ, Fagerberg B, Nielsen J, Backhed F. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 2013;498(7452):99–103. doi:10.1038/nature12198.
  • Karlsson FH, Fak F, Nookaew I, Tremaroli V, Fagerberg B, Petranovic D, Backhed F, Nielsen J. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat Commun. 2012;3:1245. doi:10.1038/ncomms2266.
  • Oh J, Byrd AL, Deming C, Conlan S, Program NCS, Kong HH, Segre JA. Biogeography and individuality shape function in the human skin metagenome. Nature. 2014;514(7520):59–64. doi:10.1038/nature13786.
  • Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, Djahanschiri B, Zeller G, Mende DR, Alberti A, et al. Ocean plankton. Structure and function of the global ocean microbiome. Science. 2015;348(6237):1261359. doi:10.1126/science.1261359.
  • Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012;28(23):3150–3152. doi:10.1093/bioinformatics/bts565.
  • Li J, Jia H, Cai X, Zhong H, Feng Q, Sunagawa S, Arumugam M, Kultima JR, Prifti E, Nielsen T, et al. An integrated catalog of reference genes in the human gut microbiome. Nat Biotechnol. 2014;32(8):834–841. doi:10.1038/nbt.2942.
  • Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, Liang S, Zhang W, Guan Y, Shen D, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55–60. doi:10.1038/nature11450.
  • Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12(1):59–60. doi:10.1038/nmeth.3176.
  • Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464(7285):59–65. doi:10.1038/nature08821.
  • Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014;42(Database issue):D199–205. doi:10.1093/nar/gkt1076.
  • Powell S, Forslund K, Szklarczyk D, Trachana K, Roth A, Huerta-Cepas J, Gabaldon T, Rattei T, Creevey C, Kuhn M, et al. eggNOG v4.0: nested orthology inference across 3686 organisms. Nucleic Acids Res. 2014;42(Database issue):D231–239. doi:10.1093/nar/gkt1253.
  • Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 2009;37(Database issue):D233–238. doi:10.1093/nar/gkn663.
  • Backhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(6):852. doi:10.1016/j.chom.2015.05.012.
  • Martinez JL, Coque TM, Baquero F. What is a resistance gene? Ranking risk in resistomes. Nat Rev Microbiol. 2015;13(2):116–123. doi:10.1038/nrmicro3399.
  • Liu B, Pop M. ARDB–antibiotic resistance genes database. Nucleic Acids Res. 2009;37(Database issue):D443–447. doi:10.1093/nar/gkn656.
  • Forsberg KJ, Patel S, Gibson MK, Lauber CL, Knight R, Fierer N, Dantas G. Bacterial phylogeny structures soil resistomes across habitats. Nature. 2014;509(7502):612–616. doi:10.1038/nature13377.
  • Broaders E, Gahan CG, Marchesi JR. Mobile genetic elements of the human gastrointestinal tract: potential for spread of antibiotic resistance genes. Gut Microbes. 2013;4(4):271–280. doi:10.4161/gmic.24627.
  • Parnanen K, Karkman A, Hultman J, Lyra C, Bengtsson-Palme J, Larsson DGJ, Rautava S, Isolauri E, Salminen S, Kumar H, et al. Maternal gut and breast milk microbiota affect infant gut antibiotic resistome and mobile genetic elements. Nat Commun. 2018;9(1):3891. doi:10.1038/s41467-018-06393-w.
  • Mardanov AV, Babykin MM, Beletsky AV, Grigoriev AI, Zinchenko VV, Kadnikov VV, Kirpichnikov MP, Mazur AM, Nedoluzhko AV, Novikova ND, et al. Metagenomic analysis of the dynamic changes in the gut microbiome of the participants of the MARS-500 experiment, simulating long term space flight. Acta Naturae. 2013;5(3):116–125. doi:10.32607/20758251-2013-5-3-116-125.
  • Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489(7415):242–249. doi:10.1038/nature11552.
  • Russell WR, Duncan SH, Scobbie L, Duncan G, Cantlay L, Calder AG, Anderson SE, Flint HJ. Major phenylpropanoid-derived metabolites in the human gut can arise from microbial fermentation of protein. Mol Nutr Food Res. 2013;57(3):523–535. doi:10.1002/mnfr.201200594.
  • Lee SM, Donaldson GP, Mikulski Z, Boyajian S, Ley K, Mazmanian SK. Bacterial colonization factors control specificity and stability of the gut microbiota. Nature. 2013;501(7467):426–429. doi:10.1038/nature12447.
  • Fischbach MA, Sonnenburg JL. Eating for two: how metabolism establishes interspecies interactions in the gut. Cell Host Microbe. 2011;10(4):336–347. doi:10.1016/j.chom.2011.10.002.
  • Pokusaeva K, Fitzgerald GF, van Sinderen D. Carbohydrate metabolism in bifidobacteria. Genes Nutr. 2011;6(3):285–306. doi:10.1007/s12263-010-0206-6.
  • Presti I, D’Orazio G, Labra M, La Ferla B, Mezzasalma V, Bizzaro G, Giardina S, Michelotti A, Tursi F, Vassallo M, et al. Evaluation of the probiotic properties of new lactobacillus and bifidobacterium strains and their in vitro effect. Appl Microbiol Biotechnol. 2015;99(13):5613–5626. doi:10.1007/s00253-015-6482-8.
  • Citar M, Hacin B, Tompa G, Stempelj M, Rogelj I, Dolinsek J, Narat M, Matijasic BB. Human intestinal mucosa-associated lactobacillus and bifidobacterium strains with probiotic properties modulate IL-10, IL-6 and IL-12 gene expression in THP-1 cells. Benef Microbes. 2015;6(3):325–336. doi:10.3920/BM2014.0081.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.