The structural discrepancy between the small and large gut microbiota of Asiatic toad (Bufo gargarizans) during hibernation
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
31600104
National Natural Science Foundation of China
192102110005
Key R&D and Promotion Projects of Henan Province
PubMed
36637770
DOI
10.1007/s12223-023-01031-5
PII: 10.1007/s12223-023-01031-5
Knihovny.cz E-zdroje
- Klíčová slova
- 16S rRNA, Amphibian, Batch effect, Gut microbiome, Hibernation,
- MeSH
- hibernace * MeSH
- RNA ribozomální 16S genetika MeSH
- ropuchy genetika mikrobiologie MeSH
- střevní mikroflóra * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- RNA ribozomální 16S MeSH
Hibernating amphibians are suitable for the research on the adaptation of gut microbiota to long-term fasting and cold stresses. However, the previous studies mainly focus on the large or whole gut microbiota but not the small gut microbiota. To test the structural discrepancy between the small and large gut microbiota during hibernation, we performed two independent batches of 16S rRNA gene amplicon sequencing to profile the small and large gut microbiota of hibernating Asiatic toad (Bufo gargarizans) from two wild populations. Both batches of data revealed that Proteobacteria, Bacteroidetes, and Firmicutes were the three most dominant phyla in the small and large gut microbiota. Three core OTUs with 100% occurrence in all gut microbiotas were annotated as Pseudomonas. A significant structural discrepancy was detected between the small and large gut microbiota. For instance, Proteobacteria assembled in the small intestine with a higher proportion than it did in the large intestine, but Bacteroidetes and Firmicutes assembled in the large intestine with a higher proportion than they did in the small intestine. The large gut microbiota exhibited higher diversity than the small gut microbiota. Nevertheless, a severe batch effect existed in the structural analysis of the gut microbiotas. The large gut microbiota showed a better resistance to the batch effect than the small gut microbiota did. This study provides preliminary evidence that microbes assemble in the small and large intestines of amphibians with discrepant patterns during hibernation.
Zobrazit více v PubMed
Banas JA, Loesche WJ, Nace GW (1988) Classification and distribution of large intestinal bacteria in nonhibernating and hibernating leopard frogs (Rana pipiens). Appl Environ Microbiol 54:2305–2310. https://doi.org/10.1128/aem.54.9.2305-2310.1988 PubMed DOI PMC
Bharti R, Grimm DG (2019) Current challenges and best-practice protocols for microbiome analysis. Brief Bioinform 22:178–193. https://doi.org/10.1093/bib/bbz155 DOI PMC
Bletz MC, Goedbloed DJ, Sanchez E et al (2016) Amphibian gut microbiota shifts differentially in community structure but converges on habitat-specific predicted functions. Nat Commun 7:13699. https://doi.org/10.1038/ncomms13699 PubMed DOI PMC
Bolyen E, Rideout JR, Dillon MR et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9 PubMed DOI PMC
Boutilier RG (2001) Mechanisms of metabolic defense against hypoxia in hibernating frogs. Respir Physiol 128:365–377. https://doi.org/10.1016/S0034-5687(01)00312-7 PubMed DOI
Chai L, Dong Z, Chen A, Wang H (2018) Changes in intestinal microbiota of Bufo gargarizans and its association with body weight during metamorphosis. Arch Microbiol 200:1087–1099. https://doi.org/10.1007/s00203-018-1523-1 PubMed DOI
Che J, Wang K (2016) AmphibiaChina: an online database of Chinese Amphibians. Zool Res 37:57–59. https://doi.org/10.13918/j.issn.2095-8137.2016.1.57
Costanzo JP, do Amaral MCF, Rosendale AJ, Lee RE (2014) Seasonality of freeze tolerance in a subarctic population of the wood frog, Rana sylvatica. Intern J Zool 750153. https://doi.org/10.1155/2014/750153
Ding J, Dai R, Yang L et al (2017) Inheritance and establishment of gut microbiota in chickens. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.01967
Donaldson GP, Lee SM, Mazmanian SK (2016) Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 14:20–32. https://doi.org/10.1038/nrmicro3552 PubMed DOI
Geiser F (2013) Hibernation. Curr Biol 23:R188–R193. https://doi.org/10.1016/j.cub.2013.01.062 PubMed DOI
Guo X, Chen F, Gao F et al (2020) CNSA: a data repository for archiving omics data. Database 2020. https://doi.org/10.1093/database/baaa055
Jiang H-Y, Ma J-E, Li J et al (2017) Diets alter the gut microbiome of crocodile lizards. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.02073
Kim D, Hofstaedter CE, Zhao C et al (2017) Optimizing methods and dodging pitfalls in microbiome research. Microbiome 5:52. https://doi.org/10.1186/s40168-017-0267-5 PubMed DOI PMC
Kim KK, Lee J-S, Stevens DA (2013) Microbiology and epidemiology of Halomonas species. Future Microbiol 8:1559–1573. https://doi.org/10.2217/fmb.13.108 PubMed DOI
Knight R, Vrbanac A, Taylor BC et al (2018) Best practices for analysing microbiomes. Nat Rev Microbiol 16:410–422. https://doi.org/10.1038/s41579-018-0029-9 PubMed DOI
Knutie SA, Wilkinson CL, Kohl KD, Rohr JR (2017) Early-life disruption of amphibian microbiota decreases later-life resistance to parasites. Nat Commun 8:86. https://doi.org/10.1038/s41467-017-00119-0 PubMed DOI PMC
Kohl KD, Cary TL, Karasov WH, Dearing MD (2013) Restructuring of the amphibian gut microbiota through metamorphosis. Environ Microbiol Rep 5:899–903. https://doi.org/10.1111/1758-2229.12092 PubMed DOI
Kohl KD, Cary TL, Karasov WH, Dearing MD (2015) Larval exposure to polychlorinated biphenyl 126 (PCB-126) causes persistent alteration of the amphibian gut microbiota. Environ Toxicol Chem 34:1113–1118. https://doi.org/10.1002/etc.2905 PubMed DOI
Li J, Rui J, Li Y et al (2020) Ambient temperature alters body size and gut microbiota of Xenopus tropicalis. Sci China Life Sci 63:915–925. https://doi.org/10.1007/s11427-019-9540-y PubMed DOI
Liu C, Cui Y, Li X, Yao M (2020) microeco: an R package for data mining in microbial community ecology. FEMS Microbiol Ecol 97. https://doi.org/10.1093/femsec/fiaa255
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507 PubMed DOI PMC
Martinez-Guryn K, Leone V, Chang EB (2019) Regional diversity of the gastrointestinal microbiome. Cell Host Microbe 26:314–324. https://doi.org/10.1016/j.chom.2019.08.011 PubMed DOI PMC
Milsom WK, Jackson DC (2011) Hibernation and gas exchange. In Comprehensive Physiology pp. 397–420
Naya DE, Veloso C, Sabat P, Bozinovic F (2009) The effect of short- and long-term fasting on digestive and metabolic flexibility in the Andean toad, Bufo spinulosus. J Exp Biol 212:2167–2175. https://doi.org/10.1242/jeb.030650 PubMed DOI
Ning D, Yuan M, Wu L et al (2020) A quantitative framework reveals ecological drivers of grassland microbial community assembly in response to warming. Nat Commun 11:4717. https://doi.org/10.1038/s41467-020-18560-z PubMed DOI PMC
Oksanen J, Blanchet FG, Friendly M et al (2020) Vegan: Community Ecology Package. R package version 2.5–7
Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829. https://doi.org/10.1093/bioinformatics/bts252 PubMed DOI PMC
Regan MD, Chiang E, Liu Y et al (2022) Nitrogen recycling via gut symbionts increases in ground squirrels over the hibernation season. Science 375:460–463. https://doi.org/10.1126/science.abh2950 PubMed DOI PMC
Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. Peer J 4:e2584. https://doi.org/10.7717/peerj.2584
Salter SJ, Cox MJ, Turek EM et al (2014) Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 12:87. https://doi.org/10.1186/s12915-014-0087-z PubMed DOI PMC
Schroeder BO (2019) Fight them or feed them: how the intestinal mucus layer manages the gut microbiota. Gastroenterol Rep (oxf) 7:3–12. https://doi.org/10.1093/gastro/goy052 PubMed DOI
Schwartz C, Andrews MT (2013) Chapter nine - circannual transitions in gene expression: lessons from seasonal adaptations. In Curr Top Dev Biol (Rougvie AE, O'Connor MB eds.), pp 247–273. Academic Press
Segata N, Izard J, Waldron L et al (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60 PubMed DOI PMC
Shi Q, Zhu Y, Wang J, Yang H, Wang J, Zhu W (2019) Protein restriction and succedent realimentation affecting ileal morphology, ileal microbial composition and metabolites in weaned piglets. Animal 13:2463–2472. https://doi.org/10.1017/S1751731119000776 PubMed DOI
Sommer F, Ståhlman M, Ilkayeva O et al (2016) The gut microbiota modulates energy metabolism in the hibernating brown bear Ursus arctos. Cell Rep 14:1655–1661. https://doi.org/10.1016/j.celrep.2016.01.026 PubMed DOI
Song X, Song J, Song H, Zeng Q, Shi K (2018) A robust noninvasive approach to study gut microbiota structure of amphibian tadpoles by feces. Asian Herpetol Res 9:1–12. https://doi.org/10.16373/j.cnki.ahr.170062
Song X, Zhang J, Song J, Zhai Y (2021) Decisive effects of life stage on the gut microbiota discrepancy between two wild populations of hibernating Asiatic toads (Bufo gargarizans). Front Microbiol 12. https://doi.org/10.3389/fmicb.2021.665849
Stegen JC, Lin X, Fredrickson JK et al (2013) Quantifying community assembly processes and identifying features that impose them. ISME J 7:2069–2079. https://doi.org/10.1038/ismej.2013.93 PubMed DOI PMC
Team RC (2020) R: a language and environment for statistical computing
Tong Q, Cui L-Y, Hu Z-F, Du X-P, Abid HM, Wang H-B (2020a) Environmental and host factors shaping the gut microbiota diversity of brown frog Rana dybowskii. Sci Total Environ 741:140142. https://doi.org/10.1016/j.scitotenv.2020a.140142
Tong Q, Hu Z-F, Du X-P, Bie J, Wang H-B (2020b) Effects of seasonal hibernation on the similarities between the skin microbiota and gut microbiota of an amphibian (Rana dybowskii). Microb Ecol 79:898–909. https://doi.org/10.1007/s00248-019-01466-9 PubMed DOI
Tong Q, Liu X-N, Hu Z-F et al (2019) Effects of captivity and season on the gut microbiota of the brown frog (Rana dybowskii). Front Microbiol 10. https://doi.org/10.3389/fmicb.2019.01912
Wagener C, du Plessis M, Measey J (2021) Invasive amphibian gut microbiota and functions shift differentially in an expanding population but remain conserved across established populations. Microb Ecol. https://doi.org/10.1007/s00248-021-01896-4 PubMed DOI
Wagner Mackenzie B, Waite DW, Taylor MW (2015) Evaluating variation in human gut microbiota profiles due to DNA extraction method and inter-subject differences. Front Microbiol 6. https://doi.org/10.3389/fmicb.2015.00130
Wan X-L, McLaughlin RW, Zheng J-S et al (2018) Microbial communities in different regions of the gastrointestinal tract in East Asian finless porpoises (Neophocaena asiaeorientalis sunameri). Sci Rep 8:14142. https://doi.org/10.1038/s41598-018-32512-0 PubMed DOI PMC
Wang Y, LêCao K-A (2019) Managing batch effects in microbiome data. Brief Bioinform 21:1954–1970. https://doi.org/10.1093/bib/bbz105 DOI
Warne RW, Kirschman L, Zeglin L (2019) Manipulation of gut microbiota during critical developmental windows affects host physiological performance and disease susceptibility across ontogeny. J Anim Ecol 88:845–856. https://doi.org/10.1111/1365-2656.12973 PubMed DOI
Weng FC-H, Yang Y-J, Wang D (2016) Functional analysis for gut microbes of the brown tree frog (Polypedates megacephalus) in artificial hibernation. BMC Genomics 17:1024. https://doi.org/10.1186/s12864-016-3318-6 PubMed DOI PMC
Wesolowska-Andersen A, Bahl MI, Carvalho V et al (2014) Choice of bacterial DNA extraction method from fecal material influences community structure as evaluated by metagenomic analysis. Microbiome 2:19. https://doi.org/10.1186/2049-2618-2-19 PubMed DOI PMC
Wiebler JM, Kohl KD, Lee RE, Costanzo JP (2018) Urea hydrolysis by gut bacteria in a hibernating frog: evidence for urea-nitrogen recycling in Amphibia. Proc R Soc B Biol Sci 285:20180241. https://doi.org/10.1098/rspb.2018.0241 DOI
Xu LL, Chen H, Zhang M et al (2020) Changes in the community structure of the symbiotic microbes of wild amphibians from the eastern edge of the Tibetan Plateau. MicrobiologyOpen 9:e1004. https://doi.org/10.1002/mbo3.1004
Yang P, Hu H, Li Y et al (2019) Effect of dietary xylan on immune response, tight junction protein expression and bacterial community in the intestine of juvenile turbot (Scophthalmus maximus L.). Aquaculture 512:734361. https://doi.org/10.1016/j.aquaculture.2019.734361
Zhang M, Gaughan S, Chang Q et al (2018) Age-related changes in the gut microbiota of the Chinese giant salamander (Andrias davidianus). MicrobiologyOpen 0:e778. https://doi.org/10.1002/mbo3.778
Zhou J, Nelson TM, Rodriguez Lopez C, Sarma RR, Zhou SJ, Rollins LA (2020) A comparison of nonlethal sampling methods for amphibian gut microbiome analyses. Mol Ecol Resour 20:844–855. https://doi.org/10.1111/1755-0998.13139 PubMed DOI