Skip to main content

Advertisement

Log in

Microbial diversity and composition in different gut locations of hyperlipidemic mice receiving krill oil

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Low-dose (LD, 100 mg kg−1 day−1), moderate-dose (MD, 200 mg kg−1 day−1), and high-dose (HD, 600 mg kg−1 day−1) krill oil treatments have a stepwise, enhanced effect on alleviating hyperlipidemia, and 16S rRNA sequencing of the fecal samples demonstrates that krill oil treatment alters microbial communities. Feces may not represent all microbial communities in the gastrointestinal (GI) tract. Therefore, in this study, the stored ileal and colon samples collected from LD and HD groups were sequenced, and the location-specific modulations of microbial communities were observed after krill oil treatments. The 16S rRNA sequencing of the ileal samples showed that the LD and HD groups have similar patterns between control and high-fat diet (HFD) treatments, and six most abundant genera and 40 operational taxonomic units that respond to krill oil treatment were identified. However, the 16S rRNA sequencing of the colon samples showed that LD krill oil shifts the structure from the HFD to that of the control, whereas the HD group was distributed between the control and HFD groups. The corresponding most abundant genera and responsive OTUs totaled 4 and 45, respectively. In conclusion, different gastrointestinal tract locations contain different microbial communities. These results will help to provide a comprehensive understanding of the role of dietary krill oil in modulating the gut microbiota and alleviating hyperlipidemia.

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
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abliz A, Aji Q, Abdusalam E, Sun X, Abdurahman A, Zhou W, Moore N, Umar A (2014) Effect of Cydonia oblonga mill. Leaf extract on serum lipids and liver function in a rat model of hyperlipidaemia. J Ethnopharmacol 151(2):970–974

    Article  PubMed  Google Scholar 

  • Aderiye BI, Laleye SA, Odeyemi AT (2007) Hypolipidemic potential of Lactobacillus and Streptococcus sp. from some nigerian fermented foods. Res J Microbiol 2(6):538–544

    Article  CAS  Google Scholar 

  • Alessandra F, Annalea C, Lena B, Kjetil B, Francesco DN, Maria GA, Vincenzo Z (2012) A krill oil supplemented diet suppresses hepatic steatosis in high-fat fed rats. PLoS One 7(6):e38797

    Article  Google Scholar 

  • An HM, Park SY, Lee DK, Kim JR, Min KC, Si WL, Lim HT, Kim KJ, Ha NJ (2011) Antiobesity and lipid-lowering effects of Bifidobacterium spp. in high fat diet-induced obese rats. Lipids Health Dis 10(1):116

    Article  PubMed  PubMed Central  Google Scholar 

  • Aoki R, Kamikado K, Suda W, Takii H, Mikami Y, Suganuma N (2017) A proliferative probiotic Bifidobacterium strain in the gut ameliorates progression of metabolic disorders via microbiota modulation and acetate elevation. Sci Rep-UK 7:43522

    Article  Google Scholar 

  • Araujo P, Zhu H, Breivik JF, Hjelle JI, Zeng Y (2014) Determination and structural elucidation of triacylglycerols in krill oil by chromatographic techniques. Lipids 49(2):163–172

    Article  CAS  PubMed  Google Scholar 

  • Banni S, Carta G, Murru E, Cordeddu L, Giordano E, Sirigu AR, Berge K, Vik H, Maki KC, Di MV (2011) Krill oil significantly decreases 2-arachidonoylglycerol plasma levels in obese subjects. Nutr Metab 8(1):1–6

    Article  Google Scholar 

  • Bilgin H, Sarmis A, Tigen E, Soyletir G, Mulazimoglu L (2015) Delftia acidovorans: a rare pathogen in immunocompetent and immunocompromised patients. Can J Infect Dis Med Microbiol 26(5):277–279

    PubMed  PubMed Central  Google Scholar 

  • Bindels LB, Segura Munoz RR, Gomesneto JC, Mutemberezi V, Martínez I, Salazar N, Cody EA, Quinterovillegas MI, Kittana H, Cg RG (2017) Resistant starch can improve insulin sensitivity independently of the gut microbiota. Microbiome 5(1):12

    Article  PubMed  PubMed Central  Google Scholar 

  • Burri L, Berge K, Wibrand K, Berge RK, Barger JL (2011) Differential effects of krill oil and fish oil on the hepatic transcriptome in mice. Front Genet 2:45

    Article  PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Miao H, Feng YL, Zhao YY, Lin RC (2014) Metabolomics in dyslipidemia. Adv Clin Chem 66:101

    Article  CAS  PubMed  Google Scholar 

  • Choi JH, Kim GB, Cha CJ (2014) Spatial heterogeneity and stability of bacterial community in the gastrointestinal tracts of broiler chickens. Poultry Sci 93(8):1942–1950

    Article  CAS  Google Scholar 

  • Demir O, Sevimli S, Değirmenci H, Duman H, Bakırcı EM, Demirelli S, Hamur H (2013) Evaluation of dose efficacy of treatment with atorvastatin, rosuvastatin and simvastatin in patients with hyperlipidemia. J Am Coll Cardiol 62(18):182

    Article  Google Scholar 

  • Deutsch L (2007) Evaluation of the effect of neptune krill oil on chronic inflammation and arthritic symptoms. J Am Coll Cardiol 26(1):39

    CAS  Google Scholar 

  • Drissi F, Merhej V, Angelakis E, Kaoutari AE, Carrière F, Henrissat B, Raoult D (2014) Comparative genomics analysis of Lactobacillus species associated with weight gain or weight protection. Nutr Diabetes 4:e109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460

    Article  CAS  PubMed  Google Scholar 

  • Gu S, Chen D, Zhang JN, Lv X, Wang K, Duan LP, Nie Y, XL W (2013) Bacterial community mapping of the mouse gastrointestinal tract. PLoS One 8(10):e74957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He K, Hu Y, Ma H, Zou Z, Xiao Y, Yang Y, Feng M, Li X, Ye X (2016) Rhizoma Coptidis alkaloids alleviate hyperlipidemia in B6 mice by modulating gut microbiota and bile acid pathways. BBA-Mol Basis Dis 1862(9):1696–1709

    Article  CAS  Google Scholar 

  • Hussein G, Nakagawa T, Goto H, Shimada Y, Matsumoto K, Sankawa U, Watanabe H (2007) Astaxanthin ameliorates features of metabolic syndrome in SHR/NDmcr-cp. Life Sci 80(6):522–529

    Article  CAS  PubMed  Google Scholar 

  • Jenkins DJ, Kendall CW, Vuksan V (1999) Inulin, oligofructose and intestinal function. J Nutr 129(7 Suppl):1431S

    CAS  PubMed  Google Scholar 

  • Jiang X, Takacs-Vesbach CD (2017) Microbial community analysis of pH 4 thermal springs in Yellowstone National Park. Extremophiles Life Under Extreme Conditions 21(1):1–18

    Article  Google Scholar 

  • Khan M, Raoult D, Richet H, Lepidi H, La SB (2007) Growth-promoting effects of single-dose intragastrically administered probiotics in chickens. Br Poult Sci 48(6):732–735

    Article  CAS  PubMed  Google Scholar 

  • Kim CH, Mitchell JB, Bursill CA, Sowers AL, Thetford A, Cook JA, van Reyk DM, Davies MJ (2015) The nitroxide radical TEMPOL prevents obesity, hyperlipidaemia, elevation of inflammatory cytokines, and modulates atherosclerotic plaque composition in apoE−/− mice. Atherosclerosis 240(1):234–241

    Article  CAS  PubMed  Google Scholar 

  • Kohl KD, Miller AW, Marvin JE, Mackie R, Dearing MD (2014) Herbivorous rodents (Neotoma spp.) harbour abundant and active foregut microbiota. Environ Microbiol 16(9):2869–2878

    Article  CAS  PubMed  Google Scholar 

  • Kreutzer C, Peters S, Schulte DM, Fangmann D, Türk K, Wolff S, Van ET, Ahrens M, Beckmann J, Schafmayer C (2017) Hypothalamic inflammation in human obesity is mediated by environmental and genetic factors. Diabetes. https://doi.org/10.2337/db17-0067

  • Lau WB, Ohashi K, Wang Y, Ogawa H, Murohara T, Ma XL, Ouchi N (2017) Role of adipokines in cardiovascular disease. Circ J 81:920–928

  • Le RT, Llopis M, Lepage P, Bruneau A, Rabot S, Bevilacqua C, Martin P, Philippe C, Walker F, Bado A (2013) Intestinal microbiota determines development of non-alcoholic fatty liver disease in mice. Gut 62(12):1787–1794

    Article  Google Scholar 

  • Ley R, Turnbaugh P, Klein S, Gordon J (2006) Human gut microbes associated with obesity. Nature 444(7122):1022–1023

    Article  CAS  PubMed  Google Scholar 

  • Looft T, Allen HK, Cantarel BL, Levine UY, Bayles DO, Alt DP, Henrissat B, Stanton TB (2014) Bacteria, phages and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations. ISME J 8(8):1566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu C, Sun T, Li Y, Zhang D, Zhou J, Su X (2017a) Modulation of the gut microbiota by krill oil in mice fed a high-sugar high-fat diet. Front Microbiol 8:905. https://doi.org/10.3389/fmicb.2017.00905

  • Lu C, Zhou J, Li Y, Zhang D, Wang Z, Cheong L, Zhang C, Su X (2017b) Structural modulation of gut microbiota in Bama minipigs in response to treatment with a “growth-promoting agent”, salbutamol. Appl Microbiol Biotechnol. https://doi.org/10.1007/s00253-017-8329-y

  • Marques FZ, Nelson E, Chu PY, Horlock D, Fiedler A, Ziemann M, Tan JK, Kuruppu S, Rajapakse NW, El-Osta A, Mackay CR, Kaye DM (2017) High-fiber diet and acetate supplementation change the gut microbiota and prevent the development of hypertension and heart failure in hypertensive mice. Circulation 135(10):964–977

    Article  CAS  PubMed  Google Scholar 

  • Meuric V, Le GDS, Boyer E, Acuñaamador L, Martin B, Fong SB, Barloyhubler F, Bonnauremallet M (2017) Signature of microbial dysbiosis in periodontitis. Appl Environ Microbiol. https://doi.org/10.1128/AEM.00462-17

  • Ohkawara S, Furuya H, Nagashima K, Asanuma N, Hino T (2006) Effect of oral administration of Butyrivibrio fibrisolvens MDT-1 on experimental enterocolitis in mice. Clin Vaccine Immunol 13(11):1231–1236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sampalis F, Bunea R, Pelland MF, Kowalski O, Duguet N, Dupuis S (2003) Evaluation of the effects of neptune krill oil on the management of premenstrual syndrome and dysmenorrhea. Altern Med Rev 8(2):171

    PubMed  Google Scholar 

  • Sato B, Nakajima H, Fujita T, Takase S, Yoshimura S, Kinoshita T, Terano H (2005) FR177391, a new anti-hyperlipidemic agent from Serratia. J Antibiot 58(10):634

    Article  CAS  PubMed  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamburini S, Clemente JC (2016) Zooming in on inflammatory bowel disease: microbial and proteomic features associated with IBD in colonic microenvironments. Cell Mol Gastroen Hepatol 2(5):540–541

    Article  Google Scholar 

  • Tang WH, Kitai T, Hazen SL (2017) Gut microbiota in cardiovascular health and disease. Circ Res 120(7):1183

    Article  CAS  PubMed  Google Scholar 

  • Tomasello G, Tralongo P, Damiani P, Sinagra E, Trapani BD, Zeenny MN, Hussein IH, Jurjus A, Leone A (2014) Dismicrobism in inflammatory bowel disease and colorectal cancer: changes in response of colocytes. World J Gastroentero 20(48):18121–18130

    Article  CAS  Google Scholar 

  • Tyler AD, Knox N, Kabakchiev B, Milgrom R, Kirsch R, Cohen Z, McLeod RS, Guttman DS, Krause DO, Silverberg MS (2013) Characterization of the gut-associated microbiome in inflammatory pouch complications following ileal pouch-anal anastomosis. PLoS One 8(9):e66934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Horn DJ, Wolf CR, Colman DR, Jiang X, Kohler TJ, Mcknight DM, Stanish LF, Yazzie T, Takacsvesbach CD (2016) Patterns of bacterial biodiversity in the glacial meltwater streams of the McMurdo Dry Valleys, Antarctica. FEMS Microbiol Ecol 92(10):fiw148

    Article  PubMed  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wirth R, Bódi N, Maróti G, Bagyánszki M, Talapka P, Fekete É, Bagi Z, Kovács KL (2014) Regionally distinct alterations in the composition of the gut microbiota in rats with streptozotocin-induced diabetes. PLoS One 9(12):e110440

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu WK, Panyod S, Ho CT, Kuo CH, Wu MS, Sheen LY (2015) Dietary allicin reduces transformation of L-carnitine to TMAO through impact on gut microbiota. J Funct Foods 15:408–417

    Article  CAS  Google Scholar 

  • Xia T, Lai W, Han M, Ma X, Zhang L (2017) Dietary ZnO nanoparticles alters intestinal microbiota and inflammation response in weaned piglets. Oncotarget. 10.18632/oncotarget.17612

  • Xiao L, Si BS, Feng Q, Chen N, Xia Z, Li X, Fang Z, Zhang D, Fjære E, Midtbø LK (2017) High-fat feeding rather than obesity drives taxonomical and functional changes in the gut microbiota in mice. Microbiome 5(1):43

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiao S, Fei N, Pang X, Shen J, Wang L, Zhang B, Zhang M, Zhang X, Zhang C, Li M (2014) A gut microbiota-targeted dietary intervention for amelioration of chronic inflammation underlying metabolic syndrome. FEMS Microbiol Ecol 87(2):357–367

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Lian F, Zhao L, Zhao Y, Chen X, Zhang X, Guo Y, Zhang C, Zhou Q, Xue Z (2015) Structural modulation of gut microbiota during alleviation of type 2 diabetes with a Chinese herbal formula. ISME J 9(3):552–562

    Article  PubMed  Google Scholar 

  • Xu X, Zhang X (2015) Lentinula edodes-derived polysaccharide alters the spatial structure of gut microbiota in mice. PLoS One 10(1):e0115037

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang C (2010) Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J 4(2):232

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Ji H, Liu H, Wang S, Wang J, Wang Y (2016) Changes in the diversity and composition of gut microbiota of weaned piglets after oral administration of Lactobacillus or an antibiotic. Appl Microbiol Biotechnol 100(23):1–13

    Article  Google Scholar 

  • Zhang X, Zhao Y, Zhang M, Pang X, Xu J, Kang C, Li M, Zhang C, Zhang Z, Zhang Y (2012) Structural changes of gut microbiota during berberine-mediated prevention of obesity and insulin resistance in high-fat diet-fed rats. PLoS One 7(8):e42529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao W, Wang Y, Liu S, Huang J, Zhai Z, He C, Ding J, Wang J, Wang H, Fan W (2015) The dynamic distribution of porcine microbiota across different ages and gastrointestinal tract segments. PLoS One 10(2):e0117441

    Article  PubMed  PubMed Central  Google Scholar 

  • Zoetendal EG, Raes J, Van dBB, Arumugam M, Booijink CC, Troost FJ, Bork P, Wels M, de Vos WM, Kleerebezem M (2012) The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J 6(7):1415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by the Natural Science Foundation of Zhejiang Province (LY18C010001), General project of Zhejiang Education Department (Y20163580), K.C. Wong Magna Fund in Ningbo University. We thank Nature Research Editing Service for English language editing.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chenyang Lu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All experimental procedures and animal care were performed in accordance with the Guide for the Care and Use of Laboratory Animals prepared by the Ningbo University Laboratory Animal Center (affiliated with the Zhejiang Laboratory Animal Common Service Platform), and all the animal protocols were approved by the Ningbo University Laboratory Animal Center under permit number No. SYXK (ZHE 2008-0110).

Electronic supplementary material

ESM 1

(PDF 861 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lu, C., Sun, T., Li, Y. et al. Microbial diversity and composition in different gut locations of hyperlipidemic mice receiving krill oil. Appl Microbiol Biotechnol 102, 355–366 (2018). https://doi.org/10.1007/s00253-017-8601-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-017-8601-1

Keywords

Navigation