Effect of Microgravity on the Gut Microbiota Bacterial Composition in a Hindlimb Unloading Model
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals
2.2. The HU Mice Model
2.3. Gut Dissection and Sample Collection
2.4. Metagenomic DNA Extraction
2.5. Sequencing of the Bacterial 16 rRNA
2.6. Data Analysis
3. Results
3.1. Characteristics of Study Subjects
3.2. Composition of Microbial Community Analysis between Gravity and Microgravity Groups: Interspecific Variations in Bacterial Gut Communities
3.3. Relative Abundance of Taxa
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Barratt, M.R.; Pool, S.L. (Eds.) Principles of Clinical Medicine for Space Flight; Springer Science & Business Media: New York, NY, USA, 2008. [Google Scholar]
- Siddiqui, R.; Akbar, N.; Khan, N.A. Gut microbiome and human health under the space environment. J. Appl. Microbiol. 2021, 130, 14–24. [Google Scholar] [CrossRef] [PubMed]
- Saei, A.A.; Barzegari, A. The microbiome: The forgotten organ of the astronaut’s body–probiotics beyond terrestrial limits. Future Microbiol. 2012, 7, 1037–1046. [Google Scholar] [CrossRef] [PubMed]
- Garrett-Bakelman, F.E.; Darshi, M.; Green, S.J.; Gur, R.C.; Lin, L.; Macias, B.R.; Mckenna, M.J.; Meydan, C.; Mishra, T.; Nasrini, J.; et al. The NASA Twins Study: A multidimensional analysis of a year-long human spaceflight. Science 2019, 364, eaau8650. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Zhang, Y.; Guo, J.; Kang, L.; Deng, Y.; Li, Y. Investigation on rat intestinal homeostasis alterations induced by 7-day simulated microgravity effect based on a proteomic approach. Acta Astronaut. 2020, 166, 560–566. [Google Scholar] [CrossRef]
- Li, P.; Shi, J.; Zhang, P.; Wang, K.; Li, J.; Liu, H.; Zhou, Y.; Xu, X.; Hao, J.; Sun, X.; et al. Simulated microgravity disrupts intestinal homeostasis and increases colitis susceptibility. FASEB J. 2015, 29, 3263–3273. [Google Scholar] [CrossRef]
- Shi, J.; Wang, Y.; He, J.; Li, P.; Jin, R.; Wang, K.; Xu, X.; Hao, J.; Zhang, Y.; Liu, H.; et al. Intestinal microbiota contributes to colonic epithelial changes in simulated microgravity mouse model. FASEB J. 2017, 31, 3695–3709. [Google Scholar] [CrossRef] [Green Version]
- Voorhies, A.A.; Lorenzi, H.A. The challenge of maintaining a healthy microbiome during long-duration space missions. Front. Astron. Space Sci. 2016, 3, 23. [Google Scholar] [CrossRef] [Green Version]
- Turroni, S.; Rampelli, S.; Biagi, E.; Consolandi, C.; Severgnini, M.; Peano, C.; Quercia, S.; Soverini, M.; Carbonero, F.G.; 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, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Chowdhury, P.; Long, A.; Harris, G.; Soulsby, M.E.; Dobretsov, M. Animal model of simulated microgravity: A comparative study of hindlimb unloading via tail versus pelvic suspension. Physiol. Rep. 2013, 1, e00012. [Google Scholar] [CrossRef]
- Globus, R.K.; Morey-Holton, E. Hindlimb unloading: Rodent analog for microgravity. J. Appl. Physiol. 2016, 120, 1196–1206. [Google Scholar] [CrossRef]
- Dutta, S.; Sengupta, P. Men and mice: Relating their ages. Life Sci. 2016, 152, 244–248. [Google Scholar] [CrossRef] [PubMed]
- Kovacs, G.T.A.; Shadden, M. Analysis of age as a factor in NASA astronaut selection and career landmarks. PLoS ONE 2017, 12, e0181381. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baek, H.; Cho, M.; Kim, S.; Hwang, H.; Song, M.; Yoo, S. Analysis of length of hospital stay using electronic health records: A statistical and data mining approach. PLoS ONE 2018, 13, e0195901. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brocca, L.; Pellegrino, M.A.; Desaphy, J.-F.; Pierno, S.; Camerino, D.C.; Bottinelli, R. Is oxidative stress a cause or consequence of disuse muscle atrophy in mice? A proteomic approach in hindlimb-unloaded mice: Proteomic analysis of disused mouse muscles. Exp. Physiol. 2010, 95, 331–350. [Google Scholar] [CrossRef] [Green Version]
- Shama, S.; Qaisar, R.; Khan, N.A.; Tauseef, I.; Siddiqui, R. The Role of 4-Phenylbutyric Acid in Gut Microbial Dysbiosis in a Mouse Model of Simulated Microgravity. Life 2022, 12, 1301. [Google Scholar] [CrossRef]
- Xia, Y.; Chen, F.; Du, Y.; Liu, C.; Bu, G.; Xin, Y.; Liu, B. A modified SDS-based DNA extraction method from raw soybean. Biosci. Rep. 2019, 39, BSR20182271. [Google Scholar] [CrossRef] [Green Version]
- Youssef, N.; Sheik, C.S.; Krumholz, L.R.; Najar, F.Z.; Roe, B.A.; Elshahed, M.S. Comparison of species richness estimates obtained using nearly complete fragments and simulated pyrosequencing-generated fragments in 16S rRNA gene-based environmental surveys. Appl. Environ. Microbiol. 2009, 75, 5227–5236. [Google Scholar] [CrossRef] [Green Version]
- Caporaso, J.G.; Lauber, C.L.; Walters, W.A.; Berg-Lyons, D.; Lozupone, C.A.; Turnbaugh, P.J.; Fierer, N.; Knight, R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA 2011, 108 (Suppl. S1), 4516–4522. [Google Scholar] [CrossRef] [Green Version]
- Hess, M.; Sczyrba, A.; Egan, R.; Kim, T.-W.; Chokhawala, H.; Schroth, G.; Luo, S.; Clark, D.S.; Chen, F.; Zhang, T.; et al. Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 2011, 331, 463–467. [Google Scholar] [CrossRef] [Green Version]
- Bolyen, E.; Rideout, J.R.; Dillon, M.R.; Bokulich, N.A.; Abnet, C.C.; Al-Ghalith, G.A.; Alexander, H.; Alm, E.J.; Arumugam, M.; Asnicar, F.; et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 2019, 37, 852–857. [Google Scholar] [CrossRef]
- Bull, M.J.; Plummer, N.T. Part 1: The human gut microbiome in health and disease. Integr. Med. 2014, 13, 17–22. [Google Scholar]
- Valdes, A.; Walter, J.; Segal, E.; Spector, T.D. Role of the gut microbiota in nutrition and health. BMJ 2018, 361, k2179. [Google Scholar] [CrossRef] [Green Version]
- Kang, D.-W.; Adams, J.B.; Gregory, A.C.; Borody, T.; Chittick, L.; Fasano, A.; Khoruts, A.; Geis, E.; Maldonado, J.; McDonough-Means, S.; et al. Microbiota Transfer Therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: An open-label study. Microbiome 2017, 5, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Kelly, J.R.; Minuto, C.; Cryan, J.F.; Clarke, G.; Dinan, T.G. Cross talk: The microbiota and neurodevelopmental disorders. Front. Neurosci. 2017, 11, 490. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ghoshal, U.C.; Shukla, R.; Ghoshal, U.; Gwee, K.A.; Ng, S.C.; Quigley, E.M. The gut microbiota and irritable bowel syndrome: Friend or foe? Int. J. Inflamm. 2012, 2012, 151085. [Google Scholar] [CrossRef] [PubMed]
- Siddiqui, R.; Maciver, S.; Elmoselhi, A.; Soares, N.C.; Khan, N.A. Longevity, cellular senescence and the gut microbiome: Lessons to be learned from crocodiles. Heliyon 2021, 7, e08594. [Google Scholar] [CrossRef]
- Karim, A.; Qaisar, R.; Azeem, M.; Jose, J.; Ramachandran, G.; Ibrahim, Z.M.; Elmoselhi, A.; Ahmad, F.; Abdel-Rahman, W.M.; Ranade, A.V. Hindlimb unloading induces time-dependent disruption of testicular histology in mice. Sci. Rep. 2022, 12, 17406. [Google Scholar] [CrossRef]
- Lloyd, S.A.; Lang, C.H.; Zhang, Y.; Paul, E.M.; Laufenberg, L.J.; Lewis, G.S.; Donahue, H.J. Interdependence of muscle atrophy and bone loss induced by mechanical unloading. J. Bone Miner. Res. 2014, 29, 1118–1130. [Google Scholar] [CrossRef] [Green Version]
- Langille, M.G.; Meehan, C.J.; Koenig, J.E.; Dhanani, A.S.; Rose, R.A.; Howlett, S.E.; Beiko, R.G. Microbial shifts in the aging mouse gut. Microbiome 2014, 5, 50. [Google Scholar] [CrossRef] [Green Version]
- Jackson, S.J.; Andrews, N.; Ball, D.; Bellantuono, I.; Gray, J.; Hachoumi, L.; Holmes, A.; Latcham, J.; Petrie, A.; Potter, P.; et al. Does age matter? The impact of rodent age on study outcomes. Lab. Anim. 2016, 51, 160–169. [Google Scholar] [CrossRef] [Green Version]
- Ley, R.E.; Turnbaugh, P.J.; Klein, S.; Gordon, J.I. Human gut microbes associated with obesity. Nature 2006, 444, 1022–1023. [Google Scholar] [CrossRef] [PubMed]
- Zhai, R.; Xue, X.; Zhang, L.; Yang, X.; Zhao, L.; Zhang, C. Strain-specific anti-inflammatory properties of two Akkermansia muciniphila strains on chronic colitis in mice. Front. Cell. Infect. Microbiol. 2019, 9, 239. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mukherjee, A.; Lordan, C.; Ross, R.P.; Cotter, P.D. Gut microbes from the phylogenetically diverse genus Eubacterium and their various contributions to gut health. Gut Microbes 2020, 12, 1802866. [Google Scholar] [CrossRef]
- Jalanka-Tuovinen, J.; Salonen, A.; Nikkilä, J.; Immonen, O.; Kekkonen, R.; Lahti, L.; Palva, A.; De Vos, W.M. Intestinal microbiota in healthy adults: Temporal analysis reveals individual and common core and relation to intestinal symptoms. PLoS ONE 2011, 6, e23035. [Google Scholar] [CrossRef] [PubMed]
- Stojanov, S.; Berlec, A.; Štrukelj, B. The influence of probiotics on the Firmicutes/Bacteroidetes ratio in the treatment of obesity and inflammatory bowel disease. Microorganisms 2020, 8, 1715. [Google Scholar] [CrossRef]
Species | Mean | Variance | SE | Mean | Variance | SE | p Value |
---|---|---|---|---|---|---|---|
Akkermansia muciniphila | 0.03397 | 0.000305 | 0.010088 | 0.000896 | 5.32 × 10−7 | 0.000421 | 0.004909 |
Eubacterium coprostanoligenes | 0.00446 | 5.00 × 10−6 | 0.00129 | 0.000354 | 2.27 × 10−9 | 2.75 × 10−5 | 0.006939 |
Bacteroides acidifaciens | 0.00083 | 1.17 × 10−7 | 0.000197 | 3.79 × 10−5 | 4.30 × 10−9 | 3.79 × 10−5 | 0.00303 |
Clostridium leptum | 0.00055 | 1.42 × 10−7 | 0.000218 | 4.42 × 10−5 | 2.27 × 10−9 | 2.75 × 10−5 | 0.014111 |
Methylorubrum extorquens | 0.00018 | 2.38 × 10−8 | 8.91 × 10−5 | 0 | 0 | 0 | 0.034232 |
Comamonas testosterone | 8.84 × 10−5 | 5.14 × 10−9 | 4.14 × 10−5 | 0 | 0 | 0 | 0.018808 |
Desulfovibrio fairfieldensis | 0.0001 | 8.01 × 10−9 | 5.17 × 10−5 | 0 | 0 | 0 | 0.046788 |
Bacteroides coprocola | 8.21 × 10−5 | 5.14 × 10−9 | 4.14 × 10−5 | 0 | 0 | 0 | 0.03804 |
Aerococcus urinaeequi | 8.84 × 10−5 | 5.86 × 10−9 | 4.42 × 10−5 | 0 | 0 | 0 | 0.022596 |
Helicobacter hepaticus | 5.68 × 10−5 | 2.51 × 10−9 | 2.89 × 10−5 | 0 | 0 | 0 | 0.041848 |
Burkholderiales | 2.53 × 10−5 | 4.78 × 10−10 | 1.26 × 10−5 | 0 | 0 | 0 | 0.022596 |
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Siddiqui, R.; Qaisar, R.; Khan, N.A.; Alharbi, A.M.; Alfahemi, H.; Elmoselhi, A. Effect of Microgravity on the Gut Microbiota Bacterial Composition in a Hindlimb Unloading Model. Life 2022, 12, 1865. https://doi.org/10.3390/life12111865
Siddiqui R, Qaisar R, Khan NA, Alharbi AM, Alfahemi H, Elmoselhi A. Effect of Microgravity on the Gut Microbiota Bacterial Composition in a Hindlimb Unloading Model. Life. 2022; 12(11):1865. https://doi.org/10.3390/life12111865
Chicago/Turabian StyleSiddiqui, Ruqaiyyah, Rizwan Qaisar, Naveed Ahmed Khan, Ahmad M. Alharbi, Hasan Alfahemi, and Adel Elmoselhi. 2022. "Effect of Microgravity on the Gut Microbiota Bacterial Composition in a Hindlimb Unloading Model" Life 12, no. 11: 1865. https://doi.org/10.3390/life12111865