Skip to main content

Advertisement

Log in

A Metagenomic Study of Intestinal Microbial Diversity in Relation to Feeding Habits of Surface and Cave-Dwelling Sinocyclocheilus Species

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Light is completely absent in cave habitats, causing a shortage or lack of autochthonous photosynthesis. Thus, understanding the mechanisms underlying the ability of organisms to adapt to the unique cave habitat is of great interest. We used high-throughput sequencing of the 16S ribosomal RNA gene of intestinal microorganisms from 11 Sinocyclocheilus (Cypriniformes: Cyprinidae) species, to explore the characteristics of intestinal microorganisms and the adaptive mechanisms of Sinocyclocheilus cavefish and surface fish. We found that the α-diversity and richness of the intestinal microbiome were much higher in cavefish than in surface fish. Principal coordinate analysis showed that cavefish and surface fish formed three clusters because of different dominant gut microorganisms which are generated by different habitats. Based on PICRUSt-predicted functions, harmful substance degradation pathways were much more common in cavefish intestinal microorganisms than in those from surface fish. The intestinal microbiota of surface fish group 1 had a higher capacity for carbohydrate metabolism, whereas protein and amino acid metabolism and digestive pathways were more abundant in microorganisms from the cavefish group and surface fish group 2. Combined analysis of the intestinal microbial composition and functional predictions further revealed the structures and functions of intestinal microbial communities in Sinocyclocheilus cave and surface species. Moreover, based on their habits and intestinal microbial composition and intestinal microbial functional predictions, we inferred that the three fish groups were all omnivorous; however, surface fish group 1 preferred feeding on plants, while surface fish group 2 and cavefish preferred meat. This study improves our understanding of mechanisms of adaptation in cave habitats and may contribute to the protection of these habitats from water pollution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Aspiras AC, Nicolas R, Brian M, Borowsky RL, Tabin CJ (2015) Melanocortin 4 receptor mutations contribute to the adaptation of cavefish to nutrient-poor conditions. Proc Natl Acad Sci U S A 112:1–6

    Google Scholar 

  2. Borowsky R (2018) Cavefishes. Curr Biol 28:60–64. https://doi.org/10.1016/j.cub.2017.12.011

    Article  CAS  Google Scholar 

  3. Meng F, Braasch I, Phillips JB, Lin X, Titus T, Zhang C, Postlethwait JH (2013) Evolution of the eye transcriptome under constant darkness in Sinocyclocheilus cavefish. Mol Biol Evol 30:1527–1543. https://doi.org/10.1093/molbev/mst079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Li DH, Luo TC (2002) Elemental study on species diversity of karst cave animals in Shilin area of Yunnan province. Journal of Guizhou Normal University (Natural Sciences) 20:1–5

    CAS  Google Scholar 

  5. Romero A (2001) An introduction to the special volume on the biology of hypogean fishes. In: Romero A (ed) The biology of hypogean fishes. Springer Netherlands, Dordrecht, pp 7–12

    Google Scholar 

  6. Zhao YH (2006) Past research and future development on endemic chinese cavefish of the genus sinocyclocheilus (cypriniformes,cyprinidae). Acta Zootaxon Sin 31:769–777

    Google Scholar 

  7. Sukantak N (2010) Role of gastrointestinal microbiota in fish. Aquac Res 41:1553–1573

    Google Scholar 

  8. Pond MJ, Stone DM, Alderman DJ (2006) Comparison of conventional and molecular techniques to investigate the intestinal microflora of rainbow trout ( Oncorhynchus mykiss ). Aquaculture 261:194–203

    CAS  Google Scholar 

  9. Gatesoupe FJ (2007) Live yeasts in the gut: natural occurrence, dietary introduction, and their effects on fish health and development. Aquaculture 267:20–30

    Google Scholar 

  10. Skrodenytė-Arbačiauskienė V (2000) Proteolytic activity of the roach (Rutilus Rutilus L.) intestinal microflora. Acta Zoologica Lituanica 10:69–77. https://doi.org/10.1080/13921657.2000.10512337

    Google Scholar 

  11. Skrodenyte-Arbaciauskiene V, Sruoga A, Butkauskas D (2006) Assessment of microbial diversity in the river trout Salmo trutta fario L. intestinal tract identified by partial 16S rRNA gene sequence analysis. Fish Sci 72:597–602

    CAS  Google Scholar 

  12. Gómez GD, Balcázar JL (2008) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol Med Microbiol 52:145–154. https://doi.org/10.1111/j.1574-695X.2007.00343.x

    Article  CAS  PubMed  Google Scholar 

  13. Ringø E, Olsen RE, Mayhew TM, Myklebust R (2003) Electron microscopy of the intestinal microflora of fish. Aquaculture 227:395–415. https://doi.org/10.1016/j.aquaculture.2003.05.001

    Article  Google Scholar 

  14. Jankauskienë R (2002) Defence mechanisms in fish: frequency of the genus Lactobacillus bacteria in the intestinal tract microflora of carps. Biologija 2:13–17

    Google Scholar 

  15. Bairagi A, Ghosh KS, Sen SK, Ray AK (2002) Enzyme producing bacterial flora isolated from fish digestive tracts. Aquac Int 10:109–121

    CAS  Google Scholar 

  16. Bates JM, Mittge E, Kuhlman J, Baden KN, Cheesman SE, Guillemin K (2006) Distinct signals from the microbiota promote different aspects of zebrafish gut differentiation. Dev Biol 297:374–386

    CAS  PubMed  Google Scholar 

  17. Hovda MB, Lunestad BT, Fontanillas R, Rosnes JT (2007) Molecular characterisation of the intestinal microbiota of farmed Atlantic salmon ( Salmo salar L.). Aquaculture 272:581–588

    CAS  Google Scholar 

  18. Ingerslev HC, Jørgensen LVG, Strube ML, Larsen N, Dalsgaard I, Boye M, Madsen L (2014) The development of the gut microbiota in rainbow trout ( Oncorhynchus mykiss ) is affected by first feeding and diet type. Aquacultures 424–425:24–34

    Google Scholar 

  19. Saha S, Roy RN, Sen SK, Ray AK (2006) Characterization of cellulase-producing bacteria from the digestive tract of tilapia, Oreochromis mossambica (Peters) and grass carp, Ctenopharyngodon idella (Valenciennes). Aquac Res 37:380–388

    CAS  Google Scholar 

  20. Li W, Liu Y, Yang H (2002) Two new species of Sinocycolocheilus form eastern Yunnan, China. Journal of Yunnan Agricultural University 17:58–60

    CAS  Google Scholar 

  21. Li W (1985) Four new species of sinocyclocheilus from Yunnan (cypriniformes: cyprinidae: barbinae). Zool Res 6:125–129

    CAS  Google Scholar 

  22. Li W (1992) Description on three species of sinocyclocheilus from Yunnan, China. Acta Hydrobiol Sin 16:57–61

    Google Scholar 

  23. Chu XL (1985) A revision of Chinese cyprinid genus sinocyclocheilus with reference to the interspecific relationships. Acta Zootaxon Sin 10:101–107

    Google Scholar 

  24. Li W, Mao W (2002) One new species of sinocyclocheilus from Yunnan. Journal of Zhantiang Fisheries College 22:1–3

    Google Scholar 

  25. Zhao YH, Zhang CG (2013) Validation and re-description of Sinocyclocheilus aluensis Li et Xiao, 2005 (Cypriniforms: Cyprinidae). Zool Res 34:374–378

    PubMed  Google Scholar 

  26. Li W (1994) A new species of cyprinidae from Yunnan-Sinocyclocheilus rhinocerous. Journal of Zhantiang Fisheries College 14:1–3

    CAS  Google Scholar 

  27. Li G (1989) On a new fish of the genus sinocyclocheilus from Guangxi China (cypriniformes: cyprinidae: barbinae). Zool Syst 14:126–129

    Google Scholar 

  28. Li W, Lan J (1992) A new genis and three new species of cyprinidae from Guangxi, China. Journal of Zhantiang Fisheries College 12:46–51

    Google Scholar 

  29. Chen Y, Yang J, Lan J (1997) One new species of blind cavefish from Guangxi with comments on its phylogenetic status (Cypriniformes:Cyprinidae:Barbinae). Zoological Systematics 22:219–223

    Google Scholar 

  30. Wang D, Liao J (1997) A new species of sinocyclocheilus from Guizhou, China (Cypriniformes: Cyprinidae: Barbinae). Acta Academiae Medicinae Zunyi 20:1–3

    CAS  Google Scholar 

  31. Mago T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Google Scholar 

  32. Ling Z, Li Z, Liu X, Cheng Y, Luo Y, Tong X, Yuan L, Wang Y, Sun J, Li L (2014) Altered fecal microbiota composition associated with food allergy in infants. Appl Environ Microbiol 80:2546–2554

    PubMed  PubMed Central  Google Scholar 

  33. Tsuchiya C, Sakata T, Sugita H (2010) Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish. Lett Appl Microbiol 46:43–48

    Google Scholar 

  34. Kessel MAV, Dutilh BE, Neveling K, Kwint MP, Veltman JA, Flik G, Jetten MS, Klaren PH, Camp HJOD (2011) Pyrosequencing of 16S rRNA gene amplicons to study the microbiota in the gastrointestinal tract of carp ( Cyprinus carpio L.). AMB Express 1:41–41

    PubMed  PubMed Central  Google Scholar 

  35. Wu S, Gao T, Zheng Y, Wang W, Cheng Y, Wang G (2016) Microbial diversity of intestinal contents and mucus in yellow catfish (Pelteobagrus fulvidraco). Aquaculture 303:1–7

    Google Scholar 

  36. Huang H, Wu X (1987) China economic animal record: freshwater fishes. Science Press

  37. Zhao Y, Zhang C (2009) Endemic fishes of Sinocyclocheilus (Cypriniformes:Cyprinidae) in China. Science press

  38. Li Weixian WD (1999) Biological survey of Sinocyclocheilus maitianheensis. Freshw Fish 29:23–24

    Google Scholar 

  39. Li T, Long M, Gatesoupe FJ, Zhang Q, Li A, Gong X (2015) Comparative analysis of the intestinal bacterial communities in different species of carp by pyrosequencing. Microb Ecol 69:1–12

    Google Scholar 

  40. Li W, Wu D, Chen A, Tao J (2000) The preliminary investigation of geographical distribution and ecological adaptation for cave environment of Sinocyclocheilus rhinocerous--a cyprinid fish. Journal of Yunnan Agricultural University 15:1–4

    Google Scholar 

  41. Ni J, Yu Y, Zhang T, Gao L (2012) Comparison of intestinal bacterial communities in grass carp, Ctenopharyngodon idellus, from two different habitats. Chin J Oceanol Limnol 30:757–765

    Google Scholar 

  42. Liu H, Guo X, Gooneratne R, Lai R, Zeng C, Zhan F, Wang W (2016) The gut microbiome and degradation enzyme activity of wild freshwater fishes influenced by their trophic levels. Sci Rep 6:24340. https://doi.org/10.1038/srep24340

  43. Bakkemckellep AM, Penn MH, Salas PM, Refstie S, Sperstad S, Landsverk T, Ringø E, Krogdahl A (2007) Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). Br J Nutr 97:699–713

    CAS  Google Scholar 

  44. Larsen AM, Mohammed HH, Arias CR (2014) Characterization of the gut microbiota of three commercially valuable warmwater fish species. J Appl Microbiol 116:1396–1404

    CAS  PubMed  Google Scholar 

  45. Li HE, Hao B, Xie C, Luo X, Zhang Z, Zhu X (2009) Isolation and identification of major cellulase-producing fungi in intestines of grass carp. Chin J App Environ Biol 15:414–418

    Google Scholar 

  46. Wu S, Wang G, Angert ER, Wang W, Li W, Zou H (2012) Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS One 7:e30440

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Feng X, Zhi XW, Zhu DM, Wang Y, Pang SF, Yan MY, Mei XH, Chen XX (2008) Study on digestive enzyme-producing bacteria from the digestive tract of Ctenopharyngodon idellus and Carassius auratus gibelio. Freshwater Fisheries 38:51–57

    Google Scholar 

  48. Ghosh K, Sen SK, Ray AK (2002) Characterization of bacilli isolated from the gut of rohu, Labeo rohita, fingerlings and its significance in digestion. J Appl Aquac 12:33–42. https://doi.org/10.1300/J028v12n03_04

    Google Scholar 

  49. Peixoto SB, Cladera-Olivera F, Daroit DJ, Brandelli A (2011) Cellulase-producing Bacillus strains isolated from the intestine of Amazon basin fish. Aquac Res 42:887–891

    CAS  Google Scholar 

  50. Ray AK, Ghosh K, Ringø E (2012) Enzyme-producing bacteria isolated from fish gut: a review. Aquac Nutr 18:465–492

    CAS  Google Scholar 

  51. Adlerberth I, Wold AE (2009) Establishment of the gut microbiota in Western infants. Acta Peadiatrica: Promoting Child Health 98:229–238

    CAS  Google Scholar 

  52. Laparra JM, Sanz Y (2010) Interactions of gut microbiota with functional food components and nutraceuticals. Pharmacol Res 61:219–225. https://doi.org/10.1016/j.phrs.2009.11.001

    CAS  PubMed  Google Scholar 

  53. Ran J, Chen H (1998) A survey of speleobiological studies in China. Carsologica Sinica 7:151–159

    Google Scholar 

  54. Zhang G, Yang W (2015) Correlation study between cave animal community and the cavern environment in dolomite karst area, Guizhou Province. Sichuan Journal of Zoology 34:375–382

    Google Scholar 

  55. Pemberton JM, Kidd SP, Schmidt R (1997) Secreted enzymes of Aeromonas. FEMS Microbiol Lett 152:1–10

    CAS  PubMed  Google Scholar 

  56. Culver DC, Pipan T (2009) biology of caves and other subterranean habitats. Oxford University Press 38: 309–311

  57. Monro A, Bystriakova N, Fu L, Wen F, Wei Y (2018) Discovery of a diverse cave flora in China. PLoS One 13:e0190801

    PubMed  PubMed Central  Google Scholar 

  58. Claus SP, Guillou H, Ellero-Simatos S (2016) The gut microbiota: a major player in the toxicity of environmental pollutants? NPJ Biofilms & Microbiomes 2:16003. https://doi.org/10.1038/npjbiofilms.2016.3

Download references

Funding

This study was partially supported by the National Natural Science Foundation of China (31560111) and the Hundred Oversea Talents Recruitmsent Program of Yunnan Province.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Shanyuan Chen or Heng Xiao.

Ethics declarations

Conflict of Interest

The authors declare the they have no conflicts of interest.

Electronic supplementary material

Online resource 1

The rarefaction analysis of each fish gut samples (PDF 387 kb) The rarefaction curves showing the quantity of OTUs per sample on the basis of number of reads for 33 specimens. (PNG 2308 kb)

Online resource 2

Unique OTUs in three groups of Sinocyclocheilus fish. Pie chart shows the characteristics of unique OTUs form cavefish group (a), surface fish group1(b) and surface group 2 (c) with a frequency higher than 1%. (PNG 2308 kb)

High Resolution Image (TIF 2173 kb)

Online resource 3

Significant differences in the abundance among intestinal microbes the phylum and genus levels between three group. The significant differences (*: P < 0.05; **: P < 0.0; ***: P < 0.001) of abundant at gut bacterial phylum (a) and genus (b) between three groups were calculated by Kruskal-Wallis rank-test. Three groups are represented by different colors, respectively: surface group 2(green), surface group 1(red), cave group (blue). The most abundant taxa (top10 at phylum level, top 15 at genus level) of bacteria used for compare show in the ordinate. (PNG 265 kb)

High Resolution Image (TIF 1218 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, H., Li, C., Liu, T. et al. A Metagenomic Study of Intestinal Microbial Diversity in Relation to Feeding Habits of Surface and Cave-Dwelling Sinocyclocheilus Species. Microb Ecol 79, 299–311 (2020). https://doi.org/10.1007/s00248-019-01409-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-019-01409-4

Keywords

Navigation