Abstract
Highland birds evolve multiple adaptive abilities to cope with the harsh environments; however, how they adapt to the high-altitude habitats via the gut microbiota remains understudied. Here we integrated evidences from comparative analysis of gut microbiota to explore the adaptive mechanism of black-necked crane, a typical highland bird in the Qinghai-Tibet Plateau. Firstly, the gut microbiota diversity and function was compared among seven crane species (one high-altitude species and six low-altitude species), and then among three populations of contrasting altitudes for the black-necked crane. Microbiota community diversity in black-necked crane was significantly lower than its low-altitude relatives, but higher microbiota functional diversity was observed in black-necked crane, suggesting that unique bacteria are developed and acquired due to the selection pressure of high-altitude environments. The functional microbial genes differed significantly between the low- and high-altitude black-necked cranes, indicating that altitude significantly impacted microbial communities’ composition and structure. Adaptive changes in microbiota diversity and function are observed in response to high-altitude environments. These findings provide us a new insight into the adaptation mechanism to the high-altitude environment for birds via the gut microbiota.
Key points
• The diversity and function of gut microbiota differed significantly between the low- and high-altitude crane species.
• Black-necked crane adapts to the high-altitude environment via specific gut microbiota.
• Altitude significantly impacted microbial communities’ composition and structure.
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Data availability
Data sets further supporting the conclusions of this article are included within the article and its supplemental files. The complete clean reads will submit to the NCBI BioProject database (https://www.ncbi.nlm.nih.gov/bioproject/) under accession number PRJNA826568.
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References
Ayres JS (2016) Cooperative microbial tolerance behaviors in host-microbiota mutualism. Cell 165(6):1323–1331. https://doi.org/10.1016/j.cell.2016.05.049
Barve S, Dhondt AA, Mathur VB, Cheviron ZA (2016) Life-history characteristics influence physiological strategies to cope with hypoxia in Himalayan birds. Proc Biol Sci 283(1843). https://doi.org/10.1098/rspb.2016.2201
Bo T, Song G, Tang S, Zhang M, Ma Z, Lv H, Wu Y, Zhang D, Yang L, Wang D, Lei F (2022) Incomplete concordance between host phylogeny and gut microbial community in tibetan wetland birds. Front Microbiol 13. https://doi.org/10.3389/fmicb.2022.848906
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS 2nd, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37(8):852–857. https://doi.org/10.1038/s41587-019-0209-9
Boyce AJ, Mouton JC, Lloyd P, Wolf BO, Martin TE (2020) Metabolic rate is negatively linked to adult survival but does not explain latitudinal differences in songbirds. Ecol Lett 23(4):642–652. https://doi.org/10.1111/ele.13464
Butler PJ (2016) The physiological basis of bird flight. Philos Trans R Soc Lond B Biol Sci 371(1704). https://doi.org/10.1098/rstb.2015.0384
Cao Y, Yang XZ, Zhang LJ, Li M, Yuan ML (2021) Gut bacteria communities differ between Gynaephora species endemic to different altitudes of the Tibetan Plateau. Sci Total Environ 777:146115
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6(8):1621
Cheng Y, Miller MJ, Zhang D, Xiong Y, Hao Y, Jia C, Cai T, Li SH, Johansson US, Liu Y, Chang Y, Song G, Qu Y, Lei F (2021) Parallel genomic responses to historical climate change and high elevation in East Asian songbirds. Proc Natl Acad Sci USA 118(50). https://doi.org/10.1073/pnas.2023918118
Dong S, Xu S, Zhang J, Hussain R, Lu H, Ye Y, Mehmood K, Zhang H, Shang P (2021) First report of fecal microflora of wild bar-headed goose in Tibet Plateau. Front Vet Sci 8:791461. https://doi.org/10.3389/fvets.2021.791461
Gao Y (2001) Cranes and people in China: culture, science, and conservation. The University of Texas at Austin, Ph.D
Grond K, Sandercock BK, Jumpponen A, Zeglin LH (2018) The avian gut microbiota: community, physiology and function in wild birds. J Avian Biol 49(11):e01788. https://doi.org/10.1111/jav.01788
Guo N, Wu Q, Shi F, Niu J, Zhang T, Degen AA, Fang Q, Ding L, Shang Z, Zhang Z, Long R (2021) Seasonal dynamics of diet-gut microbiota interaction in adaptation of yaks to life at high altitude. Npj Biofilms Microbi 7(1):38. https://doi.org/10.1038/s41522-021-00207-6
Hao Y, Xiong Y, Cheng Y, Song G, Jia C, Qu Y, Lei F (2019) Comparative transcriptomics of 3 high-altitude passerine birds and their low-altitude relatives. Proc Natl Acad Sci USA 116(24):11851–11856. https://doi.org/10.1073/pnas.1819657116
Harris J, Mirande C (2013) A global overview of cranes: status, threats and conservation priorities. Chinese Birds 4(3):189–209. https://doi.org/10.5122/cbirds.2013.0025
Ivy CM, Scott GR (2015) Control of breathing and the circulation in high-altitude mammals and birds. Comp Biochem Physiol A Mol Integr Physiol 186:66–74. https://doi.org/10.1016/j.cbpa.2014.10.009
Kindt R (2014) BiodiversityR: graphical user interface for biodiversity and community ecology analysis. R package version 2.3 (2013–01–31)
Krajewski C, Sipiorski JT, Anderson FE (2010) Complete mitochondrial genome sequences and the phylogeny of cranes (Gruiformes: Gruidae). The Auk 127(2):440-452 13
Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31(9):814–821. https://doi.org/10.1038/nbt.2676
Li C, Liu Y, Gong M, Zheng C, Zhang C, Li H, Wen W, Wang Y, Liu G (2021) Diet-induced microbiome shifts of sympatric overwintering birds. Appl Microbiol Biotechnol 105(14–15):5993–6005. https://doi.org/10.1007/s00253-021-11448-y
Liu F, Liang T, Zhang Z, Liu L, Li J, Dong W, Zhang H, Bai S, Ma L, Kang L (2021a) Effects of altitude on human oral microbes. AMB Express 11(1):41. https://doi.org/10.1186/s13568-021-01200-0
Liu K, Yang J, Yuan H (2021b) Recent progress in research on the gut microbiota and highland adaptation on the Qinghai-Tibet Plateau. J Evol Biol 34(10):1514–1530. https://doi.org/10.1111/jeb.13924
Ma Y, Ma S, Chang L, Wang H, Ga Q, Ma L, Bai Z, Shen Y, Ge R-L (2019) Gut microbiota adaptation to high altitude in indigenous animals. Biochem Bioph Res Co 516(1):120–126. https://doi.org/10.1016/j.bbrc.2019.05.085
MacInnis MJ, Rupert JL (2011) ‘ome on the range: altitude adaptation, positive selection, and Himalayan genomics. High Alt Med Biol 12(2):133–139. https://doi.org/10.1089/ham.2010.1090
McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8(4):e61217. https://doi.org/10.1371/journal.pone.0061217
McMurdie PJ, Holmes S (2015) Shiny-phyloseq: web application for interactive microbiome analysis with provenance tracking. Bioinformatics 31(2):282–283. https://doi.org/10.1093/bioinformatics/btu616
Meine C, Archibald G (1996) The cranes: status survey and conservation action plan. IUCN, Gland, Switzerland
Obeng N, Bansept F, Sieber M, Traulsen A, Schulenburg H (2021) Evolution of microbiota-host associations: the microbe’s perspective. Trends Microbiol 29(9):779–787. https://doi.org/10.1016/j.tim.2021.02.005
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin P, O’Hara RB, Simpson G, Solymos P, Henry M, Stevens H (2014) vegan: community ecology package. https://www.scienceopen.com/document?vid=bf1230d1-c04a-4ab5-b525-206c12d0c1dc. Accessed 2010
Pekarsky S, Corl A, Turjeman S, Kamath PL, Getz WM, Bowie RCK, Markin Y, Nathan R (2021) Drivers of change and stability in the gut microbiota of an omnivorous avian migrant exposed to artificial food supplementation. Mol Ecol 30(19):4723–4739. https://doi.org/10.1111/mec.16079
Qi M, Cao Z, Shang P, Zhang H, Hussain R, Mehmood K, Chang Z, Wu Q, Dong H (2021) Comparative analysis of fecal microbiota composition diversity in Tibetan piglets suffering from diarrheagenic Escherichia coli (DEC). Microb Pathog 158:105106. https://doi.org/10.1016/j.micpath.2021.105106
Qian F (2005) Conservation status of cranes in China. Forest and Humankind 25(5):8–10
Qu Y, Chen C, Chen X, Hao Y, She H, Wang M, Ericson PGP, Lin H, Cai T, Song G, Jia C, Chen C, Zhang H, Li J, Liang L, Wu T, Zhao J, Gao Q, Zhang G, Zhai W, Zhang C, Zhang YE, Lei F (2021) The evolution of ancestral and species-specific adaptations in snowfinches at the Qinghai-Tibet Plateau. P Natl Acad Sci USA 118(13). https://doi.org/10.1073/pnas.2012398118
Scanlan PD (2021) Evolution in a community context: towards understanding the causes and consequences of adaptive evolution in the human gut microbiota over short time scales. Msystems 6(4):e0083221. https://doi.org/10.1128/mSystems.00832-21
Shade A, Handelsman J (2012) Beyond the Venn diagram: the hunt for a core microbiome. Environ Microbiol 14(1):4–12. https://doi.org/10.1111/j.1462-2920.2011.02585.x
Sieber M, Traulsen A, Schulenburg H, Douglas AE (2021) On the evolutionary origins of host-microbe associations. P Natl Acad Sci USA 118(9). https://doi.org/10.1073/pnas.2016487118
Song H, Zhang Y, Gao H, Guo Y, Li S (2014) Plateau wetlands, an indispensible habitat for the black-necked crane (Grus nigricollis) — a review. Wetlands 34(4):629–639
Storz JF (2021) High-altitude adaptation: mechanistic insights from integrated genomics and physiology. Mol Biol Evol 38(7):2677–2691. https://doi.org/10.1093/molbev/msab064
Storz JF, Scott GR (2021) Phenotypic plasticity, genetic assimilation, and genetic compensation in hypoxia adaptation of high-altitude vertebrates. Comp Biochem Physiol A Mol Integr Physiol 253:110865. https://doi.org/10.1016/j.cbpa.2020.110865
Su H, Lin Y, Li D, Qian F (2000) Status of Chinese cranes and their conservation strategies. Chinese Biodiversity 8(2):180–191. https://doi.org/10.3321/j.issn:1005-0094.2000.02.007
Sundar KG, Kaur J, Choudhury BC (2000) Distribution, demography and conservation status of the Indian sarus crane (Grus antigone antigone) in India. J Bombay Nat Hist Soc 97(3):39
Tian X, Shi Q, Yu Y (2006) Status of translocation conservation of cranes in China. Chinese Wildlife 27(2):50–52. https://doi.org/10.3969/j.issn.1000-0127.2006.02.018
Trevelline BK, Fontaine SS, Hartup BK, Kohl KD (2019) Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices. Proc Biol Sci 286(1895):20182448. https://doi.org/10.1098/rspb.2018.2448
Valero-Mora P (2010) ggplot2: elegant graphics for data analysis. J Stat Softw 35. https://doi.org/10.18637/jss.v035.b01
Wang W, Wang F, Li L, Wang A, Sharshov K, Druzyaka A, Lancuo Z, Wang S, Shi Y (2020) Characterization of the gut microbiome of black-necked cranes (Grus nigricollis) in six wintering areas in China. Arch Microbiol 202(5):983–993. https://doi.org/10.1007/s00203-019-01802-0
Wei F, Wu Q, Hu Y, Huang G, Nie Y, Yan L (2019) Conservation metagenomics: a new branch of conservation biology. Sci China Life Sci 62(2):168–178. https://doi.org/10.1007/s11427-018-9423-3
Wienemann T, Schmitt-Wagner D, Meuser K, Segelbacher G, Schink B, Brune A, Berthold P (2011) The bacterial microbiota in the ceca of Capercaillie (Tetrao urogallus) differs between wild and captive birds. Syst Appl Microbiol 34(7):542–551. https://doi.org/10.1016/j.syapm.2011.06.003
Wu YH, Yao YF, Dong MM, Xia TR, Li DY, Xie M, Wu JY, Wen AX, Wang Q, Zhu GX, Ni QY, Zhang MW, Xu HL (2020) Characterisation of the gut microbial community of rhesus macaques in high-altitude environments. BMC Microbiol 20(1). https://doi.org/10.1186/s12866-020-01747-1
Zeng B, Zhang S, Xu H, Kong F, Yu X, Wang P, Yang M, Li D, Zhang M, Ni Q, Li Y, Fan X, Yang D, Ning R, Zhao J, Li Y (2020) Gut microbiota of Tibetans and Tibetan pigs varies between high and low altitude environments. Microbiol Res 235:126447. https://doi.org/10.1016/j.micres.2020.126447
Zhao J, Wang Y, Zhang M, Yao Y, Tian H, Sang Z, Wang L, Xu H (2021) Structural changes in the gut microbiota community of the black-necked crane (Grus nigricollis) in the wintering period. Arch Microbiol 203(10):6203–6214. https://doi.org/10.1007/s00203-021-02587-x
Zhou J, Lu Y, Zhang J (2012) Investigation and analysis on the current status of captive cranes in Chinese zoos. Chinese Wildlife 33(4):225–230. https://doi.org/10.3969/j.issn.1000-0127.2012.04.015
Zhu X, Guan Y, Signore AV, Natarajan C, DuBay SG, Cheng Y, Han N, Song G, Qu Y, Moriyama H, Hoffmann FG, Fago A, Lei F, Storz JF (2018) Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau. P Natl Acad Sci USA 115(8):1865–1870. https://doi.org/10.1073/pnas.1720487115
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This research was funded by the Fundamental Research Fund for the Central Non-profit Research of Chinese Academy of Forestry (Grant No. CAFYBB2020ZA004-4) and the Fundamental Research Funds for the Central Non-profit Research Institution of CAF (Grant No. CAFYBB2018QB010). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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GL and MHG conceived and designed the research. GL wrote and revised the draft. GL, CL, and YN analyzed the data. YL, CMZ, HGY, SL, XZQ, and PC collected and provided the samples. HXL, WYW, YHW, and HYQ revised the manuscript. All authors read and approved the manuscript.
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Liu, G., Li, C., Liu, Y. et al. Highland adaptation of birds on the Qinghai-Tibet Plateau via gut microbiota. Appl Microbiol Biotechnol 106, 6701–6711 (2022). https://doi.org/10.1007/s00253-022-12171-y
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DOI: https://doi.org/10.1007/s00253-022-12171-y