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

ABSTRACT Interaction between humans and the gut microbiota is important for human physiology. Here, the gut microbiota was analyzed via metagenomic sequencing, and the fluctuations in the gut microbiota under the conditions of spaceflight were characterized. The composition and function of the gut microbiota were substantially affected by spaceflight; however, individual specificity was uncompromised. We further confirmed the species fluctuations and functional genes from both missions. Resistance and virulence genes in the gut microbiota were affected by spaceflight, but the species attributions remained stable. Spaceflight markedly affected the composition and function of the human gut microbiota, implying that the human gut microbiota is sensitive to spaceflight.

[1]  Damian Szklarczyk,et al.  eggNOG v4.0: nested orthology inference across 3686 organisms , 2013, Nucleic Acids Res..

[2]  Susumu Goto,et al.  Data, information, knowledge and principle: back to metabolism in KEGG , 2013, Nucleic Acids Res..

[3]  Qiang Feng,et al.  A metagenome-wide association study of gut microbiota in type 2 diabetes , 2012, Nature.

[4]  Se Jin Song,et al.  Cohabiting family members share microbiota with one another and with their dogs , 2013, eLife.

[5]  J. Marchesi,et al.  Mobile genetic elements of the human gastrointestinal tract , 2013, Gut microbes.

[6]  Jens Roat Kultima,et al.  Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes , 2014, Nature Biotechnology.

[7]  I. Rogelj,et al.  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. , 2015, Beneficial microbes.

[8]  Fredrik H. Karlsson,et al.  Gut metagenome in European women with normal, impaired and diabetic glucose control , 2013, Nature.

[9]  B. Haribabu,et al.  Enterobacteria-secreted particles induce production of exosome-like S1P-containing particles by intestinal epithelium to drive Th17-mediated tumorigenesis , 2015, Nature Communications.

[10]  P. Degnan,et al.  Vitamin B12 as a modulator of gut microbial ecology. , 2014, Cell metabolism.

[11]  V. Tremaroli,et al.  Resource Dynamics and Stabilization of the Human Gut Microbiome during the First Year of Life Graphical Abstract Highlights , 2022 .

[12]  Michael A Fischbach,et al.  Eating for two: how metabolism establishes interspecies interactions in the gut. , 2011, Cell host & microbe.

[13]  S. Chapes Lessons from Immune 1-3: what did we learn and what do we need to do in the future? , 2004, Journal of gravitational physiology : a journal of the International Society for Gravitational Physiology.

[14]  Yangqing Peng,et al.  Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice , 2016, Nature.

[15]  A Cogoli,et al.  Activation and proliferation of lymphocytes and other mammalian cells in microgravity. , 1997, Advances in space biology and medicine.

[16]  Brandi L. Cantarel,et al.  The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics , 2008, Nucleic Acids Res..

[17]  Ruifu Yang,et al.  Increased biofilm formation ability in Klebsiella pneumoniae after short‐term exposure to a simulated microgravity environment , 2016, MicrobiologyOpen.

[18]  Francine E. Garrett-Bakelman,et al.  The NASA Twins Study: A multidimensional analysis of a year-long human spaceflight , 2019, Science.

[19]  L. Mermel,et al.  Infection prevention and control during prolonged human space travel. , 2013, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[20]  Chao Xie,et al.  Fast and sensitive protein alignment using DIAMOND , 2014, Nature Methods.

[21]  V. Tremaroli,et al.  Functional interactions between the gut microbiota and host metabolism , 2012, Nature.

[22]  Zhengwei Zhu,et al.  CD-HIT: accelerated for clustering the next-generation sequencing data , 2012, Bioinform..

[23]  Alan Feiveson,et al.  Study of the impact of long-duration space missions at the International Space Station on the astronaut microbiome , 2019, Scientific Reports.

[24]  Rob Knight,et al.  Longitudinal analysis of microbial interaction between humans and the indoor environment , 2014, Science.

[25]  David M Klaus,et al.  Antibiotic efficacy and microbial virulence during space flight. , 2006, Trends in biotechnology.

[26]  Rob Knight,et al.  Temporal variability is a personalized feature of the human microbiome , 2014, Genome Biology.

[27]  Beiwen Zheng,et al.  Alterations of the human gut microbiome in liver cirrhosis , 2014, Nature.

[28]  Jens Roat Kultima,et al.  An integrated catalog of reference genes in the human gut microbiome , 2014, Nature Biotechnology.

[29]  N. Ravin,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 , 2013, Acta naturae.

[30]  A. Hargens,et al.  Spaceflight-Induced Intracranial Hypertension and Visual Impairment: Pathophysiology and Countermeasures. , 2018, Physiological reviews.

[31]  Christian Lesterlin,et al.  Role of AcrAB-TolC multidrug efflux pump in drug-resistance acquisition by plasmid transfer , 2019, Science.

[32]  S. Rampelli,et al.  Temporal dynamics of the gut microbiota in people sharing a confined environment, a 520-day ground-based space simulation, MARS500 , 2017, Microbiome.

[33]  J. Bengtsson-Palme,et al.  Maternal gut and breast milk microbiota affect infant gut antibiotic resistome and mobile genetic elements , 2018, Nature Communications.

[34]  S. Turroni,et al.  Dynamic efficiency of the human intestinal microbiota , 2015, Critical reviews in microbiology.

[35]  Fredrik H. Karlsson,et al.  Symptomatic atherosclerosis is associated with an altered gut metagenome , 2012, Nature Communications.

[36]  J. W. Wilson,et al.  Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq , 2007, Proceedings of the National Academy of Sciences.

[37]  G. Sonnenfeld Extreme environments and the immune system: effects of spaceflight on immune responses. , 2001, The Journal of allergy and clinical immunology.

[38]  P. Bork,et al.  Enterotypes of the human gut microbiome , 2011, Nature.

[39]  F. Bäckhed,et al.  Signals from the gut microbiota to distant organs in physiology and disease , 2016, Nature Medicine.

[40]  Klaus Ley,et al.  Bacterial colonization factors control specificity and stability of the gut microbiota , 2013, Nature.

[41]  Teresa M. Coque,et al.  What is a resistance gene? Ranking risk in resistomes , 2014, Nature Reviews Microbiology.

[42]  F. Bäckhed,et al.  From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites , 2016, Cell.

[43]  H. Flint,et al.  Major phenylpropanoid-derived metabolites in the human gut can arise from microbial fermentation of protein. , 2013, Molecular nutrition & food research.

[44]  Luis Pedro Coelho,et al.  Structure and function of the global ocean microbiome , 2015, Science.

[45]  Allyson L. Byrd,et al.  Biogeography and individuality shape function in the human skin metagenome , 2014, Nature.

[46]  Bagher Forghani,et al.  Stress‐induced subclinical reactivation of varicella zoster virus in astronauts , 2004, Journal of medical virology.

[47]  Peter J. Turnbaugh,et al.  The microbial pharmacists within us: a metagenomic view of xenobiotic metabolism , 2016, Nature Reviews Microbiology.

[48]  M. Labra,et al.  Evaluation of the probiotic properties of new Lactobacillus and Bifidobacterium strains and their in vitro effect , 2015, Applied Microbiology and Biotechnology.

[49]  D. Sinderen,et al.  Carbohydrate metabolism in Bifidobacteria , 2011, Genes & Nutrition.

[50]  J. Walter,et al.  The human gut microbiome: ecology and recent evolutionary changes. , 2011, Annual review of microbiology.

[51]  D. Pierson,et al.  Asymptomatic reactivation and shed of infectious varicella zoster virus in astronauts , 2008, Journal of medical virology.

[52]  A. Macpherson,et al.  How nutrition and the maternal microbiota shape the neonatal immune system , 2017, Nature Reviews Immunology.

[53]  Wei Wang,et al.  Faecalibacterium prausnitzii (ATCC 27766) has preventive and therapeutic effects on chronic unpredictable mild stress-induced depression-like and anxiety-like behavior in rats , 2019, Psychoneuroendocrinology.

[54]  L. Duan,et al.  Gut microbes in correlation with mood: case study in a closed experimental human life support system , 2016, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[55]  P. Bork,et al.  A human gut microbial gene catalogue established by metagenomic sequencing , 2010, Nature.

[56]  D. Kasper,et al.  How colonization by microbiota in early life shapes the immune system , 2016, Science.

[57]  Mihai Pop,et al.  ARDB—Antibiotic Resistance Genes Database , 2008, Nucleic Acids Res..

[58]  Molly K. Gibson,et al.  Bacterial phylogeny structures soil resistomes across habitats , 2014, Nature.

[59]  Jian Wang,et al.  SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler , 2012, GigaScience.