Opportunistic pathogens are abundant in the gut of cultured giant spiny frog (Paa spinosa)

Aquaculture Research

Volumn 49, Issue 5, 2018, Pages 2033-2041

  Xiang, Jianguo ^a   He, Tuoyu ^a   Wang, Pengpeng ^b   Xie, Min ^b   Xiang, Jing ^b   Ni, Jiajia ^c  

^a HUNAN AGRICULTURAL UNIVERSITY   (China)

^b Hunan Fisheries Science Institute   (China)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

gut microbiota; high throughput sequencing; metagenomics; Paa spinosa; risk prediction

Indexed keywords

ANURA; BACTEROIDALES; BACTEROIDES; CETOBACTERIUM; CLOSTRIDIALES; FAECALIBACTERIUM; OTUS; PAA SPINOSA; RIKENELLACEAE; UNIDENTIFIED BACTERIUM;

EID: 85043459799     PISSN: 1355557X     EISSN: 13652109     Source Type: Journal    
DOI: 10.1111/are.13660     Document Type: Article

References (63)

1. Anderson, M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
2. Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., … Bertalan, M. (2011). Enterotypes of the human gut microbiome. Nature, 473, 174–180. https://doi.org/10.1038/nature09944
3. Atarashi, K., Tanoue, T., Shima, T., Imaoka, A., Kuwahara, T., Momose, Y., … Honda, K. (2011). Induction of colonic regulatory T cells by indigenous Clostridium species. Science, 331, 337–341. https://doi.org/10.1126/science.1198469
4. Bizzarro, S., Laine, M. L., Buijs, M. J., Brandt, B. W., Crielaard, W., Loos, B. G., & Zaura, E. (2016). Microbial profiles at baseline and not the use of antibiotics determine the clinical outcome of the treatment of chronic periodontitis. Scientific Reports, 6, 20205. https://doi.org/10.1038/srep20205
5. Bletz, M. C., Goedbloed, D. J., Sanchez, E., Reinhardt, T., Tebbe, C. C., Bhuju, S., … Steinfartz, S. (2016). Amphibian gut microbiota shifts differentially in community structure but converges on habitat-specific predicted functions. Nature Communications, 7, 13699. https://doi.org/10.1038/ncomms13699
6. Caipang, C. M. A., Brinchmann, M. F., & Kiron, V. (2010). Antagonistic activity of bacterial isolates from intestinal microbiota of Atlantic cod, Gadus morhua, and an investigation of their immunomodulatory capabilities. Aquaculture Research, 41, 249–256. https://doi.org/10.1111/j.1365-2109.2009.02327.x
7. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., … Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335–336. https://doi.org/10.1038/nmeth.f.303
8. Chan, H. K., Shoemaker, K. T., & Karraker, N. E. (2014). Demography of Quasipaa frogs in China reveals high vulnerability to widespread harvest pressure. Biological Conservation, 170, 3–9. https://doi.org/10.1016/j.biocon.2013.12.014
9. Cho, J. I., Joo, I. S., Choi, J. H., Jung, K. H., Choi, E. J., Han, M. K., … Hwang, I. G. (2013). Prevalence and antimicrobial resistance of Enterococcus spp. isolated from meat and fishery production in Korea. Food Science and Biotechnology, 22, 161–165. https://doi.org/10.1007/s10068-013-0022-z
10. Colombo, B. M., Scalvenzi, T., Benlamara, S., & Pollet, N. (2015). Microbiota and mucosal immunity in amphibians. Frontiers in Immunology, 6, 111. https://doi.org/10.3389/fimmu.2015.00111
11. Darine, T., Alaeddine, C., Fethi, B., & Ridha, M. (2015). Fluazifop-P-butyl (herbicide) affects richness and structure of soil bacterial communities. Soil Biology and Biochemistry, 81, 89–97. https://doi.org/10.1016/j.soilbio.2014.10.030
12. De Angelis, M., Piccolo, M., Vannini, L., Siragusa, S., De Giacomo, A., Serrazzanetti, D. I., … Francavilla, R. (2013). Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PLoS ONE, 8, e76993. https://doi.org/10.1371/journal.pone.0076993
13. Dixon, P. (2003). VEGAN, a package of R functions for community ecology. Journal of Vegetation Science, 14, 927–930. https://doi.org/10.1111/j.1654-1103.2003.tb02228.x
14. Dong, B. J., Zhan, Z. G., Zheng, R. Q., Chen, W., & Min, J. J. (2015). cDNA cloning and functional characterisation of four antimicrobial peptides from Paa spinosa. Zeitschrift für Naturforschung C, 70, 251–256. https://doi.org/10.1515/znc-2015-4220
15. Edgar, R. C. (2013). UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10, 996–998. https://doi.org/10.1038/nmeth.2604
16. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., & Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27, 2194–2200. https://doi.org/10.1093/bioinformatics/btr381
17. Escobar, J. S., Klotz, B., Valdes, B. E., & Agudelo, G. M. (2014). The gut microbiota of Colombians differs from that of Americans Europeans and Asians. BMC Microbiology, 14, 311. https://doi.org/10.1186/s12866-014-0311-6
18. Falony, G., Joossens, M., Vieira-Silva, S., Wang, J., Darzi, Y., Faust, K., … Raes, J. (2016). Population-level analysis of gut microbiome variation. Science, 352, 560–564. https://doi.org/10.1126/science.aad3503
19. Han, S., Liu, Y., Zhou, Z., He, S., Cao, Y., Shi, P., … Ringø, E. (2010). Analysis of bacterial diversity in the intestine of grass carp (Ctenopharyngodon idellus) based on 16S rDNA gene sequences. Aquaculture Research, 42, 47–56. https://doi.org/10.1111/j.1365-2109.2010.02543.x
20. Huang, H., Yang, G., Ye, S. P., Zhang, J. Y., & Zheng, R. Q. (2013). Phylogeographic analyses strongly suggest cryptic speciation in the giant spiny frog (Dicroglossidae: Paa spinosa) and interspecies hybridization in Paa. PLoS ONE, 8, e70403. https://doi.org/10.1371/journal.pone.0070403
21. Kohl, K. D., Cary, T. L., Karasov, W. H., & Dearing, M. D. (2013). Restructuring of the amphibian gut microbiota through metamorphosis. Environmental Microbiology Reports, 5, 899–903. https://doi.org/10.1111/1758-2229.12092
22. La-ongkham, O., Nakphaichit, M., Leelavatcharamas, V., Keawsompong, S., & Nitisinprasert, S. (2015). Distinct gut microbiota of healthy children from two different geographic regions of Thailand. Archives of Microbiology, 197, 561–573. https://doi.org/10.1007/s00203-015-1089-0
23. Li, H., Qu, J., Li, T., Li, J., Lin, Q., & Li, X. (2016). Pika population density is associated with the composition and diversity of gut microbiota. Frontiers in Microbiology, 7, 758. https://doi.org/10.3389/fmicb.2016.00758
24. Liptak, R., Celec, P., & Gardlik, R. (2016). Beneficial effects of live and dead Salmonella-based vector strain on the course of colitis in mice. Letters in Applied Microbiology, 63, 340–346. https://doi.org/10.1111/lam.12632
25. Liu, C. T., Yu, B. G., Zheng, R. Q., & Zhang, Y. (2010). Geographic variation in body size and sexual size dimorphism in the giant spiny frog Paa spinosa (David, 1875) (Anura: Ranoidae). Journal of Natural History, 44, 1729–1741. https://doi.org/10.1080/00222931003632682
26. Ma, Y. L., Guo, T., Xu, Z. R., You, P., & Ma, J. F. (2006). Effect of Lactobacillus isolates on the adhesion of pathogens to chicken intestinal mucus in vitro. Letters in Applied Microbiology, 42, 369–374. https://doi.org/10.1111/j.1472-765X.2006.01844.x
27. Magoc, T., & Salzberg, S. L. (2011). FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27, 2957–2963. https://doi.org/10.1093/bioinformatics/btr507
28. Mazmanian, S. K., Liu, C. H., Tzianabos, A. O., & Kasper, D. L. (2005). An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell, 122, 107–118. https://doi.org/10.1016/j.cell.2005.05.007
29. Mei, Q., Ye, R., Song, T., Zhao, M., & Zheng, S. (2015). Farming status and development countermeasure of P. spinosa in Zhejiang province. Zhejiang Agriculture Science, 56, 1122–1125.(in Chinese) https://doi.org/10.16178/j.issn.0528-9017.20150757
30. Miquel, S., Martín, R., Rossi, O., Bermúdez-Humarán, L. G., Chatel, J. M., Sokol, H., … Langella, P. (2013). Faecalibacterium prausnitzii and human intestinal health. Current Opinion in Microbiology, 16, 255–261. https://doi.org/10.1016/j.mib.2013.06.003
31. Ni, J., Li, X., He, Z., & Xu, M. (2017). A novel method to determine the minimum number of sequences required for reliable microbial community analysis. Journal of Microbiological Methods, 139, 196–201. https://doi.org/10.1016/j.mimet.2017.06.006
32. Ni, J. J., Yan, Q. Y., Yu, Y. H., Wu, H. H., & Chen, F. (2017). Dispersal patterns of endogenous bacteria among grass carp (Ctenopharyngodon idellus) guts. Iranian Journal of Fisheries Sciences, 16, 605–618.
33. Ni, J., Yan, Q., Yu, Y., & Zhang, T. (2014). Factors influencing the grass carp gut microbiome and its effect on metabolism. FEMS Microbiology Ecology, 87, 704–714. https://doi.org/10.1111/1574-6941.12256
34. Parks, D. H., Tyson, G. W., Hugenholtz, P., & Beiko, R. G. (2014). STAMP: Statistical analysis of taxonomic and functional profiles. Bioinformatics, 30, 3123–3124. https://doi.org/10.1093/bioinformatics/btu494
35. Qiu, Y., Kuang, X., Shi, X., Yuan, X., & Guo, R. (2014). Paludibacter jiangxiensis sp. nov., a strictly anaerobic, propionate-producing bacterium isolated from rice paddy field. Archives of Microbiology, 196, 149–155. https://doi.org/10.1007/s00203-013-0951-1
36. R Core Team (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. URL http://www.R-project.org/.
37. Reid, K. C., Cockerill III, F. R., & Patel, R. (2001). Clinical and epidemiological features of Enterococcus casseliflavus/flavescens and Enterococcus gallinarum bacteremia: A report of 20 cases. Clinical Infections Diseases, 32, 1540–1546. https://doi.org/10.1086/320542
38. Rishi, E., Rishi, P., Bhende, P., Raman, R., Sen, P., Susvar, P., … Hirawat, R. (2017). Enterococcus faecalis endophthalmitis in children - a 21 year study. Ocular Immunology and Inflammation, 13, 1–7. https://doi.org/10.1080/09273948.2017.1385816
39. Ruengsomwong, S., La-Ongkham, O., Jiang, J., Wannissom, B., Nakayama, J., & Nitisinprasert, S. (2016). Microbial community of healthy Thai vegetarians and non-vegetarians, their core gut microbiota, and pathogen risk. Journal of Microbiology and Biotechnology, 26, 1723–1735. https://doi.org/10.4014/jmb.1603.03057
40. Salmerón, I. (2017). Fermented cereal beverages: From probiotic, prebiotic and synbiotic towards Nanoscience designed healthy drinks. Letters in Applied Microbiology, 65, 114–124. https://doi.org/10.1111/lam.12740
41. Schwartz, S., Friedberg, I., Ivanov, I. V., Davidson, L. A., Goldsby, J. S., Dahl, D. B., … Chapkin, R. S. (2012). A metagenomic study of diet-dependent interaction between gut microbiota and host in infants reveals differences in immune response. Genome Biology, 13, r32. https://doi.org/10.1186/gb-2012-13-4-r32
42. Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., & Huttenhower, C. (2011). Metagenomic biomarker discovery and explanation. Genome Biology, 12, R60. https://doi.org/10.1186/gb-2011-12-6-r60
43. Shin, H., Sim, M., Lee, J., & Shin, D. (2016). Lifestyle and geographic insights into the distinct gut microbiota in elderly women from two different geographic locations. Journal of Physiological Anthropology, 35, 31. https://doi.org/10.1186/s40101-016-0121-7
44. Shu, M. (2000). An analysis of the nutritive compositions in muscle of Rana spinosa (I): Contents of normal nutrients and composition of fatty acids. Journal of Zhejiang University (Sciences Edition), 27, 433–437. (in Chinese with English abstract).
45. Shu, M., Tu, D., Zhang, P., Long, C., Gu, W., & Zhou, Z. (2017). Heat shock protein 90 is a stress and immune response gene in the giant spiny frog Quasipaa spinosa. Fisheries Science, 83, 251–258. https://doi.org/10.1007/s12562-017-1063-7
46. Song, T. (2015). Quasipaa Spinosa Scale Farming Common Disease Pathogen Identification and Vaccine Research. Hangzhou: Zhejiang Normal University.
47. Song, T., Zheng, R., Zhang, J., Jie, Z., Dong, B., & Zhao, M. (2014). A new type of Quasipaa spinosa disease pathogen analysis. Journal of Fujian Fisheries, 36, 244–250. (in Chinese with English abstract) https://doi.org/10.14012/j.cnki.fjsc.2014.05.002
48. Stappenbeck, T. S., & Virgin, H. W. (2016). Accounting for reciprocal host-microbiome interactions in experimental science. Nature, 534, 191–199. https://doi.org/10.1038/nature18285
49. Sun, D., Jiang, X., Wu, Q. L., & Zhou, N. (2013). Intragenomic heterpgeneity of 16S rRNA genes causes overestimation of prokaryotic diversity. Applied and Environmental Microbiology, 79, 5962–5969. https://doi.org/10.1128/AEM.01282-13
50. Tamaki, H., Wright, C. L., Li, X., Lin, Q., Hwang, C., Wang, S., … Liu, W. (2011). Analysis of 16S rRNA amplicon sequencing options on the Roche/454 next-generation titanium sequencing platform. PLoS ONE, 6, e25263. https://doi.org/10.1371/journal.pone.0025263
51. Teanpaisan, R., Piwat, S., & Dahlén, G. (2011). Inhibitory effect of oral Lactobacillus against oral pathogens. Letters in Applied Microbiology, 53, 452–459. https://doi.org/10.1111/j.1472-765X.2011.03132.x
52. Ulluwishewa, D., Anderson, R. C., Young, W., McNabb, W. C., van Baarlen, P., Moughan, P. J., … Roy, N. C. (2014). Live Faecalibacterium prausnitzii in an apical anaerobic model of the intestinal epithelial barrier. Cellular Microbiology, 17, 226–240. https://doi.org/10.1111/cmi.12360
53. Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73, 5261–5267. https://doi.org/10.1128/AEM.00062-07
54. Wang, A. R., Ran, C., Ringø, E., & Zhou, Z. G. (2017). Progress in fish gastrointestinal microbiota research. Reviews in Aquaculture, https://doi.org/10.1111/raq.12191
55. Wang, R., & Xiong, X. (2012). Isolation, identification and drug sensitivity tests of Proteus mirabilis from rotten-skin disease of Rana spinosa. Freshwater Fisheries, 42, 31–34.
56. Wang, H., Zhang, W., Zuo, L., Dong, J., Zhu, W., Li, Y., … Li, J. (2013). Intestinal dysbacteriosis contributes to decreased intestinal mucosal barrier function and increased bacterial translocation. Letters in Applied Microbiology, 58, 384–392. https://doi.org/10.1111/lam.12201
57. Wexler, H. M. (2007). Bacteroides: The good, the bad, and the nitty-gritty. Clinical Microbiology Reviews, 20, 593–621. https://doi.org/10.1128/CMR.00008-07
58. Wu, S., Wang, G., Angert, W., Wang, W., Li, W., & Zou, H. (2012). Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS ONE, 7, e30440. https://doi.org/10.1371/journal.pone.0030440
59. Xia, Z., Bai, E., Wang, Q., Gao, D., Zhou, J., Jiang, P., & Wu, J. (2016). Biogeographic distribution patterns of bacteria in Typical chinese forest soils. Frontiers in Microbiology, 7, 1106. https://doi.org/10.3389/fmicb.2016.01106
60. Yu, D., Zheng, R., Lu, Q., Yang, G., Fu, Y., & Zhang, Y. (2016). Genetic diversity and population structure for the conservation of giant spiny frog (Quasipaa spinosa) using microsatellite loci and mitochondrial DNA. Asian Herpetolological Research, 7, 75–86. https://doi.org/10.16373/j.cnki.ahr.150040
61. Yu, X. Y., Zheng, R. Q., Zhang, J. Y., Shen, B., & Dong, B. J. (2014). Genetic polymorphism of major histocompatibility complex class IIB alleles and pathogen resistance in the giant spiny frog Quasipaa spinosa. Infection, Genetics and Evolution, 28, 175–182. https://doi.org/10.1016/j.meegid.2014.09.028
62. Zeng, T., Ye, Y., Mu, C., Wang, K., Li, R., & Wang, C. (2016). Gut microbiota and metabolic phenotype of Portunus trituberculatus. Chinese Jounral of Analytical Chemistry, 44, 1867–1873. (in Chinese with English abstract) https://doi.org/10.1016/s1872-2040(16)60978-7
63. Zhang, C., Zhang, M., Wang, S., Han, R., Cao, Y., Hua, W., … Zhao, L. (2010). Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. The ISME Journal, 4, 32–41. https://doi.org/10.1038/ismej.2009.112