OpenLB
Open Library of Bioscience
Advanced Search
Frontiers in microbiology
2024;15 1476845.

Altitude shapes gut microbiome composition accounting for diet, thyroid hormone levels, and host genetics in a subterranean blind mole rat.

Halil Mert Solak, Jakub Kreisinger, Dagmar Čížková, Efe Sezgin, Lucie Schmiedová, Marine Murtskhvaladze, Yoshiyuki Henning, Faruk Çolak, Ferhat Matur, Alexey Yanchukov
Author Information
  1. Halil Mert Solak: Department of Biology, Faculty of Science, Bülent Ecevit University, Zonguldak, Türkiye.
  2. Jakub Kreisinger: Department of Zoology, Charles University, Prague, Czechia.
  3. Dagmar Čížková: Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Brno, Czechia.
  4. Efe Sezgin: Department of Food Engineering, Izmir Institute of Technology, Izmir, Türkiye.
  5. Lucie Schmiedová: Department of Zoology, Charles University, Prague, Czechia.
  6. Marine Murtskhvaladze: Institute of Ecology, Ilia State University, Tbilisi, Georgia.
  7. Yoshiyuki Henning: Institute of Physiology, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.
  8. Faruk Çolak: Department of Biology, Faculty of Science, Bülent Ecevit University, Zonguldak, Türkiye.
  9. Ferhat Matur: Department of Biology, Dokuz Eylül University, İzmir, Türkiye.
  10. Alexey Yanchukov: Department of Biology, Faculty of Science, Bülent Ecevit University, Zonguldak, Türkiye.
PMID: 39552645 DOI: 10.3389/fmicb.2024.1476845

Abstract

The animal gut microbiome acts as a crucial link between the host and its environment, playing a vital role in digestion, metabolism, physiology, and fitness. Using 16S rRNA metabarcoding, we investigated the effect of altitude on the microbiome composition of Anatolian Blind Mole Rats () across six locations and three altitudinal groups. We also factored in the host diet, as well as host microsatellite genotypes and thyroid hormone levels. The altitude had a major effect on microbiome composition, with notable differences in the relative abundance of several bacterial taxa across elevations. Contrary to prior research, we found no significant difference in strictly anaerobic bacteria abundance among altitudinal groups, though facultatively anaerobic bacteria were more prevalent at higher altitudes. Microbiome alpha diversity peaked at mid-altitude, comprising elements from both low and high elevations. The beta diversity showed significant association with the altitude. Altitude had a significant effect on the diet composition but not on its alpha diversity. No distinct altitude-related genetic structure was evident among the host populations, and no correlation was revealed between the host genetic relatedness and microbiome composition nor between the host microbiome and the diet. Free thyroxine (FT4) levels increased almost linearly with the altitude but none of the bacterial ASVs were found to be specifically associated with hormone levels. Total thyroxine (TT4) levels correlated positively with microbiome diversity. Although we detected correlation between certain components of the thyroid hormone levels and the microbiome beta diversity, the pattern of their relationship remains inconclusive.

Keywords

16S 18S altitude adaptation blind mole rats diet gut microbiome high altitude thyroid

References

  1. Front Microbiol. 2016 Jul 27;7:1169 [PMID: 27512391]
  2. Nucleic Acids Res. 2013 Jan 7;41(1):e1 [PMID: 22933715]
  3. J Pediatr (Rio J). 2022 Mar-Apr;98 Suppl 1:S32-S37 [PMID: 34742719]
  4. PLoS One. 2014 Mar 11;9(3):e90731 [PMID: 24618913]
  5. Environ Monit Assess. 1996 Sep;42(1-2):113-31 [PMID: 24193496]
  6. Front Integr Neurosci. 2018 Jun 12;12:21 [PMID: 29946243]
  7. Biosci Microbiota Food Health. 2021;40(1):50-58 [PMID: 33520569]
  8. Cell Metab. 2023 Mar 7;35(3):504-516.e5 [PMID: 36889284]
  9. Front Microbiol. 2016 May 18;7:758 [PMID: 27242770]
  10. Integr Zool. 2022 May;17(3):379-395 [PMID: 35051309]
  11. Cell Res. 2020 Jun;30(6):492-506 [PMID: 32433595]
  12. Nutrients. 2014 Dec 24;7(1):17-44 [PMID: 25545101]
  13. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3321-3 [PMID: 4519626]
  14. BMC Microbiol. 2009 Jun 09;9:123 [PMID: 19508720]
  15. Nat Commun. 2021 Aug 26;12(1):5141 [PMID: 34446709]
  16. BMC Microbiol. 2020 Mar 26;20(1):68 [PMID: 32216756]
  17. Science. 2008 Jun 20;320(5883):1647-51 [PMID: 18497261]
  18. Proc Natl Acad Sci U S A. 2007 Jan 16;104(3):979-84 [PMID: 17210919]
  19. Front Microbiol. 2023 Feb 23;14:1067240 [PMID: 36910187]
  20. Ecol Evol. 2020 Apr 03;10(11):4677-4690 [PMID: 32551052]
  21. Zoolog Sci. 2020 Feb;37(1):31-41 [PMID: 32068372]
  22. Oecologia. 2021 Jan;195(1):213-223 [PMID: 33458802]
  23. Microb Ecol. 2015 Feb;69(2):434-43 [PMID: 25524570]
  24. Front Microbiol. 2021 Sep 06;12:699797 [PMID: 34552569]
  25. Mol Ecol. 2019 Jul;28(13):3197-3207 [PMID: 31141224]
  26. Front Microbiol. 2016 Jul 14;7:1031 [PMID: 27471494]
  27. Nat Methods. 2016 Jul;13(7):581-3 [PMID: 27214047]
  28. Front Microbiol. 2016 Aug 17;7:1269 [PMID: 27582734]
  29. Nutrients. 2020 Jun 12;12(6): [PMID: 32545596]
  30. Microb Biotechnol. 2019 Sep;12(5):976-992 [PMID: 31380612]
  31. Evolution. 2014 Jan;68(1):48-62 [PMID: 24102503]
  32. PLoS One. 2013 Apr 22;8(4):e61217 [PMID: 23630581]
  33. Nat Rev Gastroenterol Hepatol. 2022 Oct;19(10):625-637 [PMID: 35641786]
  34. J Innate Immun. 2023;15(1):782-803 [PMID: 37899025]
  35. High Alt Med Biol. 2008 Summer;9(2):148-57 [PMID: 18578646]
  36. Int J Mol Sci. 2022 Oct 17;23(20): [PMID: 36293284]
  37. Int J Sport Nutr Exerc Metab. 2019 May 1;29(3):249-253 [PMID: 29989465]
  38. Front Microbiol. 2022 Jul 05;13:703183 [PMID: 35865927]
  39. J Clin Med. 2023 Mar 13;12(6): [PMID: 36983217]
  40. Front Microbiol. 2016 Aug 30;7:1357 [PMID: 27625642]
  41. BMC Bioinformatics. 2014 Jun 12;15:182 [PMID: 24925680]
  42. Mol Ecol Resour. 2015 May;15(3):557-61 [PMID: 25186958]
  43. BMC Immunol. 2017 Jan 6;18(1):2 [PMID: 28061847]
  44. Pharmacol Res. 2013 Mar;69(1):52-60 [PMID: 23147033]
  45. PeerJ. 2014 Mar 04;2:e281 [PMID: 24688859]
  46. Bioinformatics. 2019 Feb 1;35(3):526-528 [PMID: 30016406]
  47. Genome Res. 2015 Oct;25(10):1558-69 [PMID: 26260972]
  48. PLoS One. 2015 Oct 05;10(10):e0139633 [PMID: 26436773]
  49. World J Mens Health. 2020 Jan;38(1):48-60 [PMID: 30929328]
  50. Gut Microbes. 2016 Jul 3;7(4):313-322 [PMID: 27355107]
  51. ISME J. 2013 Apr;7(4):707-17 [PMID: 23190729]
  52. Nature. 2012 May 09;486(7402):222-7 [PMID: 22699611]
  53. Gut. 2022 Apr;71(4):734-745 [PMID: 34006584]
  54. ISME J. 2011 Oct;5(10):1595-608 [PMID: 21472014]
  55. Biomed Environ Sci. 2018 Dec;31(12):898-901 [PMID: 30636661]
  56. Biochem Biophys Res Commun. 2019 Aug 13;516(1):120-126 [PMID: 31196622]
  57. Microb Ecol. 2011 Feb;61(2):423-8 [PMID: 21181142]
  58. Hum Hered. 1993 Jan-Feb;43(1):45-52 [PMID: 8514326]
  59. Front Physiol. 2019 Apr 16;10:428 [PMID: 31057420]
  60. Microbiol Res. 2020 May;235:126447 [PMID: 32114362]
  61. OMICS. 2020 Oct;24(10):592-601 [PMID: 32907488]
  62. Rev Endocr Metab Disord. 2024 Feb;25(1):215-237 [PMID: 37824030]
  63. J Therm Biol. 2023 Jul;115:103618 [PMID: 37399744]
  64. Oecologia. 1989 Jun;79(4):496-505 [PMID: 28313484]
  65. J Mammal. 2019 May 23;100(3):910-922 [PMID: 31138949]
  66. Psychometrika. 2017 Dec;82(4):1052-1077 [PMID: 27738957]
  67. Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6 [PMID: 23193283]
  68. Biochem J. 2017 May 16;474(11):1823-1836 [PMID: 28512250]
  69. Cell Microbiol. 2021 Aug;23(8):e13338 [PMID: 33813807]
  70. Integr Comp Biol. 2017 Oct 1;57(4):756-769 [PMID: 28992216]
  71. Mol Ecol. 2019 May;28(9):2378-2390 [PMID: 30346069]
  72. Sci Rep. 2017 Dec 5;7(1):16982 [PMID: 29209019]
  73. Biol Sex Differ. 2018 Jun 18;9(1):26 [PMID: 29914546]
  74. BMC Microbiol. 2017 May 22;17(1):120 [PMID: 28532414]
  75. Nature. 2024 Jan;625(7996):813-821 [PMID: 38172637]
  76. Mamm Genome. 2021 Aug;32(4):263-281 [PMID: 34159422]
  77. PLoS One. 2018 Sep 12;13(9):e0203701 [PMID: 30208088]
  78. Int J Mol Sci. 2020 Apr 24;21(8): [PMID: 32344721]
  79. Microb Ecol. 2018 Aug;76(2):565-577 [PMID: 29372281]
  80. Genome Biol. 2010;11(10):R106 [PMID: 20979621]
  81. ISME J. 2023 Nov;17(11):1953-1965 [PMID: 37673969]
  82. Trends Endocrinol Metab. 2019 Aug;30(8):479-490 [PMID: 31257166]
  83. Annu Rev Public Health. 2021 Apr 1;42:277-292 [PMID: 33798404]
  84. Sci Rep. 2015 Oct 07;5:14682 [PMID: 26443005]
  85. Curr Biol. 2016 Jul 25;26(14):1873-9 [PMID: 27321997]
  86. Curr Biol. 2012 Dec 18;22(24):2350-4 [PMID: 23219722]
  87. Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14691-6 [PMID: 20679230]
  88. ISME J. 2021 Sep;15(9):2601-2613 [PMID: 33731838]
  89. Eur J Intern Med. 2024 Jan;119:13-30 [PMID: 37802720]
  90. Genome Med. 2021 Jan 20;13(1):10 [PMID: 33472701]
  91. J Helminthol. 1971;45(2):161-9 [PMID: 5123696]
  92. Appl Environ Microbiol. 2011 Oct;77(20):7433-7 [PMID: 21873488]
  93. Ann Bot. 2004 Aug;94(2):199 [PMID: 15229127]
  94. Compr Physiol. 2016 Jun 13;6(3):1387-428 [PMID: 27347897]
  95. Med Sci Sports Exerc. 1982;14(1):36-40 [PMID: 7070255]
  96. Cancer Res. 1967 Feb;27(2):209-20 [PMID: 6018555]
  97. NPJ Biofilms Microbiomes. 2021 Apr 20;7(1):38 [PMID: 33879801]
  98. Integr Comp Biol. 2017 Oct 1;57(4):690-704 [PMID: 28985326]
  99. Proc Biol Sci. 2020 Feb 26;287(1921):20192834 [PMID: 32097591]
  100. Cell Rep. 2016 Feb 23;14(7):1655-1661 [PMID: 26854221]
  101. Sci Rep. 2021 Nov 22;11(1):22660 [PMID: 34811423]
  102. Front Microbiol. 2017 Oct 06;8:1929 [PMID: 29056930]
  103. Bioinformatics. 2008 Jun 1;24(11):1403-5 [PMID: 18397895]
  104. BMC Pharmacol Toxicol. 2013 Dec 11;14:62 [PMID: 24325943]
  105. F1000Res. 2020 Feb 5;9: [PMID: 32076547]
  106. Front Microbiol. 2019 Apr 24;10:887 [PMID: 31105675]
  107. Front Microbiol. 2023 Feb 24;14:1136845 [PMID: 36910168]
  108. Proc Natl Acad Sci U S A. 2011 Oct 25;108(43):17714-9 [PMID: 22006317]
  109. Conserv Physiol. 2014 Mar 21;2(1):cou009 [PMID: 27293630]
  110. Nutrients. 2021 Aug 15;13(8): [PMID: 34444955]
  111. ISME J. 2013 Jul;7(7):1344-53 [PMID: 23486247]
  112. Microbiol Spectr. 2023 Dec 12;11(6):e0002023 [PMID: 37815332]
  113. Front Microbiol. 2017 Apr 25;8:725 [PMID: 28487687]
  114. Front Microbiol. 2018 Jul 26;9:1674 [PMID: 30093891]
  115. Endocr Res. 2014;39(2):79-84 [PMID: 24066698]
  116. PLoS One. 2016 May 27;11(5):e0155863 [PMID: 27232599]
  117. Genetics. 2000 Jun;155(2):945-59 [PMID: 10835412]
  118. Proc Natl Acad Sci U S A. 2014 Jul 1;111(26):E2703-10 [PMID: 24912178]
  119. ISME J. 2020 Oct;14(10):2367-2380 [PMID: 32518248]
  120. AMB Express. 2022 Jul 6;12(1):86 [PMID: 35792976]
  121. Integr Comp Biol. 2017 Oct 01;57(4):770-785 [PMID: 29048537]
  122. Physiol Rev. 2014 Apr;94(2):355-82 [PMID: 24692351]
  123. PLoS Biol. 2023 May 23;21(5):e3002117 [PMID: 37220109]
  124. Front Microbiol. 2023 Oct 12;14:1268701 [PMID: 37901817]
  125. J Anim Ecol. 2020 Nov;89(11):2415-2426 [PMID: 32858775]
  126. Curr Protoc Toxicol. 2018 Aug;77(1):e55 [PMID: 30028909]
  127. Sci Rep. 2023 Feb 22;13(1):3122 [PMID: 36813840]
  128. Front Microbiol. 2022 Nov 15;13:1062763 [PMID: 36458196]
  129. Proc Natl Acad Sci U S A. 2013 Feb 26;110(9):3229-36 [PMID: 23391737]
  130. BMC Bioinformatics. 2023 Mar 26;24(1):117 [PMID: 36967390]
  131. Sci Rep. 2014 Jun 25;4:5437 [PMID: 24961643]
  132. Child Obes. 2018 Nov/Dec;14(8):501-509 [PMID: 30183336]
  133. Bioinformatics. 2011 Aug 15;27(16):2194-200 [PMID: 21700674]
  134. AMB Express. 2021 Mar 6;11(1):41 [PMID: 33677720]
  135. Nature. 2018 Mar 8;555(7695):210-215 [PMID: 29489753]
  136. N Engl J Med. 2016 Dec 15;375(24):2369-2379 [PMID: 27974040]
Journal Article
Article has an altmetric score of 3

Word Cloud

Created with Highcharts 10.0.0microbiomehostaltitudelevelscompositiondietdiversitythyroidhormoneguteffectsignificant16SacrossaltitudinalgroupsabundancebacterialelevationsfoundanaerobicbacteriaamongalphahighbetaAltitudegeneticcorrelationthyroxineblindmoleanimalactscruciallinkenvironmentplayingvitalroledigestionmetabolismphysiologyfitnessUsingrRNAmetabarcodinginvestigatedAnatolianBlindMoleRatssixlocationsthreealsofactoredwellmicrosatellitegenotypesmajornotabledifferencesrelativeseveraltaxaContrarypriorresearchdifferencestrictlythoughfacultativelyprevalenthigheraltitudesMicrobiomepeakedmid-altitudecomprisingelementslowshowedassociationdistinctaltitude-relatedstructureevidentpopulationsrevealedrelatednessFreeFT4increasedalmostlinearlynoneASVsspecificallyassociatedTotalTT4correlatedpositivelyAlthoughdetectedcertaincomponentspatternrelationshipremainsinconclusiveshapesaccountinggeneticssubterraneanrat18Sadaptationrats

Similar Articles

Cited By