GENERAL COMMENTARY article
Commentary: Gut Microbiome and Space Travelers' Health: State of the Art and Possible Pro/Prebiotic Strategies for Long-Term Space Missions
- Department of Microbiology, Institute of Biomedicine and Translational Medicine, University of Tartu, Tartu, Estonia
by Turroni, S., Magnani, M., Kc, P., Lesnik, P., Vidal, H., and Heer, M. (2020). Front Physiol. 11:553929. doi: 10.3389/fphys.2020.553929
Recent years have shown a heightened interest in applying new technical achievements to improve the conditions for astronauts during space travels. However, there are still numerous shortcomings in the protection of space travelers' health concerning medical standards for space flight (Committee on Ethics Principles Guidelines for Health Standards for Long Duration Exploration Spaceflights et al., 2014). The paper of Turroni et al. (2020) has raised the important issue of maintaining the health and well-being of space travelers by supporting a well-functioning system of the host-microbiome in an extreme environment. Over the last 50 years, microgravity microbiome research has mainly focused on preventing gastrointestinal (GI) disturbances, as a consequence of dysbiosis due to various extreme space conditions (Gerassy-Vainberg et al., 2018; Jiang et al., 2019; Voorhies et al., 2019; Jones et al., 2020; Liu et al., 2020) and changed diets (Siddiqui et al., 2021). During space flight, dysbacteriosis with the prevalence of facultative pathogenic bacteria hampered travelers' well-being by causing inflammation and protein deficiency (Shilov et al., 1972). For the prevention of these disorders, the protective role of lactic acid bacteria in the GI tract was explored. The lactobiota of Soviet cosmonauts was investigated at the University of Tartu in Estonia, under the supervision of professor Akivo Lenzner (March 16, 1927–April 27, 2012)1 in a joint project with the Institute of Biomedical Problems of the Russian Academy of Sciences in Moscow, under the supervision of the research fellows V. M. Shilov and N. N. Lizko (Lentsner et al., 1973, 1981; Lencner et al., 1984).1
Previous Findings and their Implications for Human Deep Space Explorations
From Baikonur (former USSR, now Kazakhstan) salivary and fecal samples from the cosmonauts and trainees from various expeditions like Soyuz and Salyut were sent to Tartu. In particular, the microbiota of every cosmonaut was studied, and the lactobacilli were isolated and identified. The subsequent results were highlighted in numerous papers written in Estonian, Russian, German, and English. Key findings of this research (Lencner et al., 1984) are listed in the following:
• The baseline counts of fecal lactobacilli were log10 5.9 ± 1.3 CFU/g on MRS media;
• The composition of individual lactobiota varied across crewmembers and the most dominating species were Lactobacillus acidophilus and Lactobacillus casei;
• Compared to pre-flight, the counts of lactobacilli decreased for at least 2.0 log and that of lactic acid streptococci increased from log 4.9 ± 1.6 to 7.7 ± 0.8 CFU/g;
• Short duration flights (7 d Salut-6) seemed to have caused a decrease of dominant species of lactobacilli whereas some subordinate species of lactobacilli could be preserved;
• At the end of long duration space missions (75 and 185 d Salut-6) only the counts of L. casei decreased;
• Post-flight, in the rehabilitation period, the usually stable L. acidophilus was not found in some cosmonauts while the streptococci maintained high numbers.
Data of cosmonauts regarding the counts of lactobacilli are in line with data of healthy young terrestrial individuals (Haenel et al., 1957; Mikelsaar et al., 1972). The individuality of the microbiome, including the individuality of the lactobacilli composition, was first pointed out by the Japanese scientists Mitsuoka and Ohno (1977), and proved retrospectively with the data of 20 healthy Russian cosmonauts (Lencner et al., 1987; Mikelsaar and Mändar, 1993). At the start of short space missions (up to 1 week), the decrease from baseline values seemingly appeared to be due to the emotional stress in the extreme situations, as described previously (Holdeman et al., 1976). Some heterofermentative species of lactobacilli and lactic acid streptococci emerged in higher numbers. These discoveries have stayed valid and relevant until today. Contrary to short-term space flights, it seems that during long-term missions, changes in the composition of the lactobiota caused by the changed environment in space can be restored after a while. In Tartu, the isolated Lactobacillus strains were screened for antagonistic activity against potentially pathogenic bacteria and some other properties. Post flight, the rehabilitation period of these cosmonauts received special care to restore indigenous lactobiota. Due to the high inter-individual variability of the Lactobacillus species composition, first steps toward personalized medicine were already started in 80s. Chosen cosmonauts were provided with lyophilized cultures of their own beneficial Lactobacillus sp. strains. Three of these GI lactobacilli strains received the Russian patents in 1989 (Avtorskaja Spravka in Russian) for biological products.
Future deep space exploration missions should take the observed changes of the composition and functionality of the microbiome into account and a “well-fed” and healthy microbiome to support general well-being of crewmembers should be an important goal of dietary interventions. The value of the paper by Turroni et al. (2020) lays in renewing the ideas of probiotic strategies during long term space exploration missions. The authors have presented several probiotic products that help to protect various body functions. Recent studies have pointed toward an intricate relationship between the intestinal microbiota and the brain, forming the so called “gut-brain axis.” Lactobacillus strains have shown to produce neuroactive and neuroendocrine molecules to reduce stress-induced corticosterone and anxiety- and depression-related behavior (Bravo et al., 2011). However, the necessity for additional mechanistic studies under microgravity, including intervention studies and clinical trials are still necessary. On the contrary, the use of the individual's own protective bacteria seems a promising complementation for personalized medicine, and optimized healthcare for crewmembers. Considering usual adaptation times of the microbiome during space flight conditions, supplementation of capsulated lactobacilli would help to maintain crewmembers' gut health during the first weeks in the new space environment and during rehabilitation post-flight.
All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.
This work was supported by Estonian Research Council (Grant No. IUT34-19) and Estonian Ministry of Education and Research (Grant No. KOGU-HUMB).
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
1. ^Also written in the publications as Lencner and Lentsner.
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., et al. (2011). Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc. Natl. Acad. Sci. U.S.A. 108, 16050–16055. doi: 10.1073/pnas.1102999108
Committee on Ethics Principles Guidelines for Health Standards for Long Duration Exploration Spaceflights Board on Health Sciences Policy Institute of Medicine, Kahn, J., Liverman, C. T., and McCoy, M. A., (eds.). (2014). Health Standards for Long Duration and Exploration Spaceflight: Ethics Principles, Responsibilities, and Decision Framework. Washington, DC: National Academies Press; NASA Risk Management and Health Standards. Available online at: https://www.ncbi.nlm.nih.gov/books/NBK222156/
Gerassy-Vainberg, S., Blatt, A., Danin-Poleg, Y., Gershovich, K., Sabo, E., Nevelsky, A., et al. (2018). Radiation induces proinflammatory dysbiosis: transmission of inflammatory susceptibility by host cytokine induction. Gut 67, 97–107. doi: 10.1136/gutjnl-2017-313789
Holdeman, L. V., Good, I. J., and Moore, W. E. C. (1976). Human faecal flora: variation in bacterial composition within individuals anda possible effect of emotional stress. Appl. Environ. Microbiol. 31, 359–375. doi: 10.1128/AEM.31.3.359-375.1976
Jiang, P., Green, S. J., Chlipala, G. E., Turek, F. W., and Vitaterna, M. H. (2019). Reproducible changes in the gut microbiome suggest a shift in microbial and host metabolism during spaceflight. Microbiome 7:113. doi: 10.1186/s40168-019-0724-4
Lencner, A., Lencner, H., Brilis, V., Brilene, T., Mikelsaar, M., and Türi, M. (1987). Zur Abwehrfunktion der Laktoflora des Verdauungstraktes [The defense function of the digestive tract lactoflora]. Nahrung 31, 405–411. doi: 10.1002/food.19870310518
Lencner, A. A., Lencner, H. P., Mikelsaar, M. E., Türi, M. E., Toom, M. A., Väljaots, M. E., et al. (1984). Die quantitative Zusammensetzung der Lactoflora des Verdaaungstraktes vor und nach kosmischen Flugen unterschiedlicher Dauer [The quantitative composition of the intestinal lactoflora before and after space flights of different lengths]. Nahrung 28, 607–613. doi: 10.1002/food.19840280608
Lentsner, A. A., Lentsner, H. P., Mikelsaar, M. E., Shilov, V. M., and Lizko, N. N. (1981). Lactobacillus flora of the digestive tract of the crews of Soiuz-13 and Saliut-4. Kosm. Biol. Aviakosm. Med. 15, 39–43.
Lentsner, A. A., Shilov, V. M., Lizko, N. N., and Mikelsaar, M. E. (1973). Study of the species makeup of human intestinal lactobacilli under the conditions of a prolonged stay in an enclosed space. Kosm. Biol. Med. 7, 76–80.
Liu, Z., Luo, G., Du, R., Sun, W., Li, J., Lan, H., et al. (2020). Effects of spaceflight on the composition and function of the human gut microbiota. Gut Microbes 11, 807–819. doi: 10.1080/19490976.2019.1710091
Mikelsaar, M., and Mändar, R. (1993). “Development of individual lactic acid microflora in the human microbial ecosystem,” in Lactic Acid Bacteria, eds S. Salminen and A. von Wright (New York, NY: Marcel Dekker, Inc.), 237–293.
Shilov, V. M., Lizko, N. N., Bragina, M. P., Lencner, A. A., and Mikelsaar, M. E. (1972). “About the changes of intestinal microflora during long-term isolation of man in hermetically closed room,” in Abstracts of IV Scientific Conference of USSR (Moscow), 235–238.
Turroni, S., Magnani, M., Kc, P., Lesnik, P., Vidal, H., and Heer, M. (2020). Gut microbiome and space travelers' health: state of the art and possible pro/prebiotic strategies for long-term space missions. Front. Physiol. 11:553929. doi: 10.3389/fphys.2020.553929
Voorhies, A. A., Mark Ott, C., Mehta, S., Pierson, D. L., Crucian, B. E., Feiveson, A., et al. (2019). Study of the impact of long-duration space missions at the International Space Station on the astronaut microbiome. Sci. Rep. 9:9911. doi: 10.1038/s41598-019-46303-8
Keywords: gut microbiome, lactobacilli, probiotic, space flights, space missions
Citation: Mikelsaar M and Mändar R (2021) Commentary: Gut Microbiome and Space Travelers' Health: State of the Art and Possible Pro/Prebiotic Strategies for Long-Term Space Missions. Front. Physiol. 12:651977. doi: 10.3389/fphys.2021.651977
Received: 11 January 2021; Accepted: 01 March 2021;
Published: 23 March 2021.
Edited by:Irina Mordukhovich, Harvard University, United States
Reviewed by:Tobias Weber, European Space Agency (ESA), France
Matiram Pun, University of Calgary, Canada
Copyright © 2021 Mikelsaar and Mändar. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.