Skip to main content
Top
Published in: Urolithiasis 6/2018

01-11-2018 | Original Paper

16S rRNA gene sequencing reveals altered composition of gut microbiota in individuals with kidney stones

Authors: Ruiqiang Tang, Yonghua Jiang, Aihua Tan, Juan Ye, Xiaoying Xian, Yuanliang Xie, Qiuyan Wang, Ziting Yao, Zengnan Mo

Published in: Urolithiasis | Issue 6/2018

Login to get access

Abstract

Nephrolithiasis is a common urological disease with high prevalence and recurrence rates. Characterizing gut microbiome profiles of nephrolithiasis patients may provide valuable insights and potential biomarkers for the disease. Therefore, we explored the relation between gut microbiome and nephrolithiasis using 16S ribosomal RNA (rRNA) gene sequencing. 13 patients with multiple kidney stones and 13 matched healthy controls were recruited. A decreasing trend in number of observed species in nephrolithiasis patients was detected, although statistical significance was not reached (p = 0.086). The inter-group variability in community structure by beta diversity analysis showed a clear separation between nephrolithiasis patients and healthy controls. Twenty genera differentiated significantly in relative abundance between nephrolithiasis patients and healthy controls (all p < 0.05). Among the 20 genera, Phascolarctobacterium, Parasutterella, Ruminiclostridium_5, Erysipelatoclostridium, Fusicatenibacter and Dorea were correlated with the concentration of the trace elements in blood, including potassium, sodium, calcium and chlorinum. Characteristic microbiome in nephrolithiasis patients was also identified by linear discriminant analysis effect size (LEfSe). These findings may provide novel and non-invasive potential diagnostic biomarkers for nephrolithiasis, and contribute to prevention and treatment of nephrolithiasis from the perspective of maintaining micro-ecological equilibrium in gut.
Appendix
Available only for authorised users
Literature
1.
go back to reference Wang W, Fan J, Huang G, Li J, Zhu X, Tian Y, Su L (2017) Prevalence of kidney stones in mainland China: a systematic review. Sci Rep 7:41630CrossRef Wang W, Fan J, Huang G, Li J, Zhu X, Tian Y, Su L (2017) Prevalence of kidney stones in mainland China: a systematic review. Sci Rep 7:41630CrossRef
2.
go back to reference Attanasio M (2011) The genetic components of idiopathic nephrolithiasis. Pediatr Nephrol 26(3):337–346CrossRef Attanasio M (2011) The genetic components of idiopathic nephrolithiasis. Pediatr Nephrol 26(3):337–346CrossRef
3.
go back to reference Curhan GC (2007) Epidemiology of stone disease. Urol Clin N. Am 34(3):287–293CrossRef Curhan GC (2007) Epidemiology of stone disease. Urol Clin N. Am 34(3):287–293CrossRef
4.
go back to reference Nouvenne A, Meschi T, Prati B, Guerra A, Allegri F, Vezzoli G, Soldati L, Gambaro G, Maggiore U, Borghi L (2010) Effects of a low-salt diet on idiopathic hypercalciuria in calcium-oxalate stone formers: a 3-mo randomized controlled trial. Am J Clin Nutr 91(3):565CrossRef Nouvenne A, Meschi T, Prati B, Guerra A, Allegri F, Vezzoli G, Soldati L, Gambaro G, Maggiore U, Borghi L (2010) Effects of a low-salt diet on idiopathic hypercalciuria in calcium-oxalate stone formers: a 3-mo randomized controlled trial. Am J Clin Nutr 91(3):565CrossRef
5.
go back to reference Taylor EN, Curhan GC (2008) Fructose consumption and the risk of kidney stones. Kidney Int 73(2):207–212CrossRef Taylor EN, Curhan GC (2008) Fructose consumption and the risk of kidney stones. Kidney Int 73(2):207–212CrossRef
6.
go back to reference Leone V, Chang EB, Devkota S (2013) Diet, microbes, and host genetics: the perfect storm in inflammatory bowel diseases. J Gastroenterol 48(3):315–321CrossRef Leone V, Chang EB, Devkota S (2013) Diet, microbes, and host genetics: the perfect storm in inflammatory bowel diseases. J Gastroenterol 48(3):315–321CrossRef
7.
go back to reference Tan J, Mckenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L (2014) The role of short-chain fatty acids in health and disease. Adv Immunol 121:91–119CrossRef Tan J, Mckenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L (2014) The role of short-chain fatty acids in health and disease. Adv Immunol 121:91–119CrossRef
8.
go back to reference Taylor EN, Stampfer MJ, Curhan GC (2005) Obesity, weight gain, and the risk of kidney stones. Jama 293(4):455–462CrossRef Taylor EN, Stampfer MJ, Curhan GC (2005) Obesity, weight gain, and the risk of kidney stones. Jama 293(4):455–462CrossRef
9.
go back to reference Taylor EN, Stampfer MJ, Curhan GC (2005) Diabetes mellitus and the risk of nephrolithiasis. Kidney Int 68(3):1230–1235CrossRef Taylor EN, Stampfer MJ, Curhan GC (2005) Diabetes mellitus and the risk of nephrolithiasis. Kidney Int 68(3):1230–1235CrossRef
10.
go back to reference Obligado SH, Goldfarb DS (2008) The association of nephrolithiasis with hypertension and obesity: a review. Am J Hypertens 21(3):257–264CrossRef Obligado SH, Goldfarb DS (2008) The association of nephrolithiasis with hypertension and obesity: a review. Am J Hypertens 21(3):257–264CrossRef
11.
go back to reference Saucier NA, Sinha MK, Liang KV, Krambeck AE, Weaver AL, Bergstralh EJ, Li X, Rule AD, Lieske JC (2010) Risk factors for CKD in persons with kidney stones: a case-control study in Olmsted County, Minnesota. Am J Kidney Dis 55(1):61–68CrossRef Saucier NA, Sinha MK, Liang KV, Krambeck AE, Weaver AL, Bergstralh EJ, Li X, Rule AD, Lieske JC (2010) Risk factors for CKD in persons with kidney stones: a case-control study in Olmsted County, Minnesota. Am J Kidney Dis 55(1):61–68CrossRef
12.
go back to reference Stern JM, Moazami S, Qiu Y, Kurland I, Chen Z, Agalliu I, Burk R, Davies KP (2016) Evidence for a distinct gut microbiome in kidney stone formers compared to non-stone formers. Urolithiasis 44(5):399–407CrossRef Stern JM, Moazami S, Qiu Y, Kurland I, Chen Z, Agalliu I, Burk R, Davies KP (2016) Evidence for a distinct gut microbiome in kidney stone formers compared to non-stone formers. Urolithiasis 44(5):399–407CrossRef
13.
go back to reference Suryavanshi MV, Bhute SS, Jadhav SD, Bhatia MS, Gune RP, Shouche YS (2016) Hyperoxaluria leads to dysbiosis and drives selective enrichment of oxalate metabolizing bacterial species in recurrent kidney stone endures. Sci Rep 6:34712CrossRef Suryavanshi MV, Bhute SS, Jadhav SD, Bhatia MS, Gune RP, Shouche YS (2016) Hyperoxaluria leads to dysbiosis and drives selective enrichment of oxalate metabolizing bacterial species in recurrent kidney stone endures. Sci Rep 6:34712CrossRef
14.
go back to reference Hatch M (2017) Gut microbiota and oxalate homeostasis. Ann Transl Med 5(2):36CrossRef Hatch M (2017) Gut microbiota and oxalate homeostasis. Ann Transl Med 5(2):36CrossRef
15.
go back to reference Siener R, Bangen U, Sidhu H, Honow R, von Unruh G, Hesse A (2013) The role of Oxalobacter formigenes colonization in calcium oxalate stone disease. Kidney Int 83(6):1144–1149CrossRef Siener R, Bangen U, Sidhu H, Honow R, von Unruh G, Hesse A (2013) The role of Oxalobacter formigenes colonization in calcium oxalate stone disease. Kidney Int 83(6):1144–1149CrossRef
16.
go back to reference Magwira CA, Kullin B, Lewandowski S, Rodgers A, Reid SJ, Abratt VR (2012) Diversity of faecal oxalate-degrading bacteria in black and white South African study groups: insights into understanding the rarity of urolithiasis in the black group. J Appl Microbiol 113(2):418–428CrossRef Magwira CA, Kullin B, Lewandowski S, Rodgers A, Reid SJ, Abratt VR (2012) Diversity of faecal oxalate-degrading bacteria in black and white South African study groups: insights into understanding the rarity of urolithiasis in the black group. J Appl Microbiol 113(2):418–428CrossRef
17.
go back to reference Tang Z, Jiang S, Li J, Li X, Zhong M, Huang R, Li P, Zou A (2014) Correlation analysis between renal calculus and dietary factors in Gongcheng Yao ethnic group. J Clin Urology (China) 29(11):1018–1021 (In Chinese) Tang Z, Jiang S, Li J, Li X, Zhong M, Huang R, Li P, Zou A (2014) Correlation analysis between renal calculus and dietary factors in Gongcheng Yao ethnic group. J Clin Urology (China) 29(11):1018–1021 (In Chinese)
18.
go back to reference Tang Z, Jiang S, Li J, Li X, Zhong M, Huang R, Li P, Zou A (2015) Epidemiological survey of renal calculi in adult Yao population in Guangxi. Chin Gen Pract 18(14):1691–1694 (In Chinese) Tang Z, Jiang S, Li J, Li X, Zhong M, Huang R, Li P, Zou A (2015) Epidemiological survey of renal calculi in adult Yao population in Guangxi. Chin Gen Pract 18(14):1691–1694 (In Chinese)
19.
go back to reference Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336CrossRef Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336CrossRef
20.
go back to reference Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41 (Database issue):D590–D596PubMed Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41 (Database issue):D590–D596PubMed
21.
go back to reference Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):R60CrossRef Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):R60CrossRef
22.
go back to reference Langille MG, Zaneveld J, Caporaso JG, Mcdonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31(9):814–821CrossRef Langille MG, Zaneveld J, Caporaso JG, Mcdonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31(9):814–821CrossRef
23.
go back to reference Kelly JP, Curhan GC, Cave DR, Anderson TE, Kaufman DW (2011) Factors related to colonization with Oxalobacter formigenes in U.S. adults. J Endourol 25(4):673–679CrossRef Kelly JP, Curhan GC, Cave DR, Anderson TE, Kaufman DW (2011) Factors related to colonization with Oxalobacter formigenes in U.S. adults. J Endourol 25(4):673–679CrossRef
24.
go back to reference Batislam E, Yilmaz E, Yuvanc E, Kisa O, Kisa U (2012) Quantitative analysis of colonization with real-time PCR to identify the role of Oxalobacter formigenes in calcium oxalate urolithiasis. Urol Res 40(5):455–460CrossRef Batislam E, Yilmaz E, Yuvanc E, Kisa O, Kisa U (2012) Quantitative analysis of colonization with real-time PCR to identify the role of Oxalobacter formigenes in calcium oxalate urolithiasis. Urol Res 40(5):455–460CrossRef
25.
go back to reference Xian X, Xie Y, Ye J, Tang R, Jiang Y, Yao Z (2016) Quantification of oxalate-degrading bacteria in the gut of kidney stone patients using real-time PCR. Genom Appl Biol 35(9):2222–2228 (In Chinese) Xian X, Xie Y, Ye J, Tang R, Jiang Y, Yao Z (2016) Quantification of oxalate-degrading bacteria in the gut of kidney stone patients using real-time PCR. Genom Appl Biol 35(9):2222–2228 (In Chinese)
26.
go back to reference Barrbeare E, Saxena V, Hilt EE, Thomaswhite K, Schober M, Li B, Becknell B, Hains DS, Wolfe AJ, Schwaderer AL (2015) The interaction between Enterobacteriaceae and calcium oxalate deposits. PloS One 10(10):e0139575CrossRef Barrbeare E, Saxena V, Hilt EE, Thomaswhite K, Schober M, Li B, Becknell B, Hains DS, Wolfe AJ, Schwaderer AL (2015) The interaction between Enterobacteriaceae and calcium oxalate deposits. PloS One 10(10):e0139575CrossRef
27.
go back to reference Benakis C, Brea D, Caballero S, Faraco G, Moore J, Murphy M, Sita G, Racchumi G, Ling L, Pamer EG, Iadecola C, Anrather J (2016) Commensal microbiota affects ischemic stroke outcome by regulating intestinal gammadelta T cells. Nat Med 22(5):516–523CrossRef Benakis C, Brea D, Caballero S, Faraco G, Moore J, Murphy M, Sita G, Racchumi G, Ling L, Pamer EG, Iadecola C, Anrather J (2016) Commensal microbiota affects ischemic stroke outcome by regulating intestinal gammadelta T cells. Nat Med 22(5):516–523CrossRef
28.
go back to reference Russell SL, Gold MJ, Hartmann M, Willing BP, Thorson L, Wlodarska M, Gill N, Blanchet MR, Mohn WW, McNagny KM, Finlay BB (2012) Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep 13(5):440–447CrossRef Russell SL, Gold MJ, Hartmann M, Willing BP, Thorson L, Wlodarska M, Gill N, Blanchet MR, Mohn WW, McNagny KM, Finlay BB (2012) Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep 13(5):440–447CrossRef
29.
go back to reference Bashiardes S, Shapiro H, Rozin S, Shibolet O, Elinav E (2016) Non-alcoholic fatty liver and the gut microbiota. Mol Metab 5(9):782–794CrossRef Bashiardes S, Shapiro H, Rozin S, Shibolet O, Elinav E (2016) Non-alcoholic fatty liver and the gut microbiota. Mol Metab 5(9):782–794CrossRef
30.
go back to reference Huang W, Guo HL, Deng X, Zhu TT, Xiong JF, Xu YH, Xu Y (2017) Short-chain fatty acids inhibit oxidative stress and inflammation in mesangial cells induced by high glucose and lipopolysaccharide. Exp Clin Endocrinol Diabetes 125(2):98–105CrossRef Huang W, Guo HL, Deng X, Zhu TT, Xiong JF, Xu YH, Xu Y (2017) Short-chain fatty acids inhibit oxidative stress and inflammation in mesangial cells induced by high glucose and lipopolysaccharide. Exp Clin Endocrinol Diabetes 125(2):98–105CrossRef
31.
go back to reference Cattaneo A, Cattane N, Galluzzi S, Provasi S, Lopizzo N, Festari C, Ferrari C, Guerra UP, Paghera B, Muscio C, Bianchetti A, Volta GD, Turla M, Cotelli MS, Gennuso M, Prelle A, Zanetti O, Lussignoli G, Mirabile D, Bellandi D, Gentile S, Belotti G, Villani D, Harach T, Bolmont T, Padovani A, Boccardi M, Frisoni GB (2017) Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol Aging 49:60–68CrossRef Cattaneo A, Cattane N, Galluzzi S, Provasi S, Lopizzo N, Festari C, Ferrari C, Guerra UP, Paghera B, Muscio C, Bianchetti A, Volta GD, Turla M, Cotelli MS, Gennuso M, Prelle A, Zanetti O, Lussignoli G, Mirabile D, Bellandi D, Gentile S, Belotti G, Villani D, Harach T, Bolmont T, Padovani A, Boccardi M, Frisoni GB (2017) Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol Aging 49:60–68CrossRef
32.
go back to reference Lim MY, You HJ, Yoon HS, Kwon B, Lee JY, Lee S, Song YM, Lee K, Sung J, Ko G (2016) The effect of heritability and host genetics on the gut microbiota and metabolic syndrome. Gut 66(6):1031–1038CrossRef Lim MY, You HJ, Yoon HS, Kwon B, Lee JY, Lee S, Song YM, Lee K, Sung J, Ko G (2016) The effect of heritability and host genetics on the gut microbiota and metabolic syndrome. Gut 66(6):1031–1038CrossRef
33.
go back to reference Ling Z, Jin C, Xie T, Cheng Y, Li L, Wu N (2016) Alterations in the fecal microbiota of patients with HIV-1 infection: an observational study in a Chinese population. Sci Rep 6:30673CrossRef Ling Z, Jin C, Xie T, Cheng Y, Li L, Wu N (2016) Alterations in the fecal microbiota of patients with HIV-1 infection: an observational study in a Chinese population. Sci Rep 6:30673CrossRef
Metadata
Title
16S rRNA gene sequencing reveals altered composition of gut microbiota in individuals with kidney stones
Authors
Ruiqiang Tang
Yonghua Jiang
Aihua Tan
Juan Ye
Xiaoying Xian
Yuanliang Xie
Qiuyan Wang
Ziting Yao
Zengnan Mo
Publication date
01-11-2018
Publisher
Springer Berlin Heidelberg
Published in
Urolithiasis / Issue 6/2018
Print ISSN: 2194-7228
Electronic ISSN: 2194-7236
DOI
https://doi.org/10.1007/s00240-018-1037-y

Other articles of this Issue 6/2018

Urolithiasis 6/2018 Go to the issue