Abstract
Butyricicoccus pullicaecorum and Megasphaera elsdenii inhabit the human intestine and have probiotic potential. The aim of this study was to evaluate the effects of B. pullicaecorum and M. elsdenii on the lifespan of Caenorhabditis elegans. They significantly (P < 0.05) extended the lifespan of C. elegans compared with Escherichia coli OP50, a standard food for the worm. Analysis of age-related biomarkers such as lipofuscin, body size, and locomotory activity showed that they retarded aging. They all failed to extend the lifespan of daf-12 or dbl-1 loss-of-function C. elegans mutants compared with E. coli OP50-fed worms. However, the increase in lifespan was observed in daf-16, jnk-1, pmk-1, and skn-1 mutants. Moreover, they increased the resistance of C. elegans to a human pathogen, Salmonella typhimurium. In conclusion, B. pullicaecorum and M. elsdenii extend the lifespan of C. elegans via the transforming growth factor-beta (TGF-β) pathway associated with anti-inflammatory processes in the innate immune system.
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Eeckhaut V, Machiels K, Perrier C, Romero C, Maes S, Flahou B, Steppe M, Haesebrouck F, Sas B, Ducatelle R (2013) Butyricicoccus pullicaecorum in inflammatory bowel disease. Gut 62:1745–1752
Engelmann I, Pujol N (2010) Innate immunity in C. elegans. In: Söderhäll K (ed) Invertebrate immunity. Springer, New York, pp 105–121
Fisher AL, Lithgow GJ (2006) The nuclear hormone receptor DAF-12 has opposing effects on Caenorhabditis elegans lifespan and regulates genes repressed in multiple long-lived worms. Aging Cell 5:127 – 138
Geirnaert A, Steyaert A, Eeckhaut V, Debruyne B, Arends JB, Van Immerseel F, Boon N, Van de Wiele T (2014) Butyricicoccus pullicaecorum, a butyrate producer with probiotic potential, is intrinsically tolerant to stomach and small intestine conditions. Anaerobe 30:70–74
Gerisch B, Rottiers V, Li D, Motola DL, Cummins CL, Lehrach H, Mangelsdorf DJ, Antebi A (2007) A bile acid-like steroid modulates Caenorhabditis elegans lifespan through nuclear receptor signaling. Proc Natl Acad Sci USA 104:5014–5019
Gruber J, Ng LF, Poovathingal SK, Halliwell B (2009) Deceptively simple but simply deceptive—Caenorhabditis elegans lifespan studies: considerations for aging and antioxidant effects. FEBS Lett 583:3377–3387
Henning P, Horn C, Steyn D, Meissner H, Hagg F (2010) The potential of Megasphaera elsdenii isolates to control ruminal acidosis. Anim Feed Sci Technol 157:13–19
Hsin H, Kenyon C (1999) Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399:362–366
Ikeda T, Yasui C, Hoshino K, Arikawa K, Nishikawa Y (2007) Influence of lactic acid bacteria on longevity of Caenorhabditis elegans and host defense against salmonella enterica serovar enteritidis. Appl Environ Microbiol 73:6404–6409
John S, Jonathan H (1988) Methods. In: Wood WB (ed) The nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory Press, New York, pp 587–606
Komura T, Ikeda T, Yasui C, Saeki S, Nishikawa Y (2013) Mechanism underlying prolongevity induced by bifidobacteria in Caenorhabditis elegans. Biogerontology 14:73–87
Kurz CL, Ewbank JJ (2003) Caenorhabditis elegans: an emerging genetic model for the study of innate immunity. Nat Rev Genet 4:380–390
Kurz CL, Tan MW (2004) Regulation of aging and innate immunity in C. elegans. Aging cell 3:185–193
Kwon G, Lee J, Lim YH (2016) Dairy Propionibacterium extends the mean lifespan of Caenorhabditis elegans via activation of the innate immune system. Sci Rep 6:31713
Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023
Liu F, He CX, Luo LJ, Zou QL, Zhao YX, Saini R, Han SF, Knölker HJ, Wang LS, Ge BX (2013) Nuclear hormone receptor regulation of microRNAs controls innate immune responses in C. elegans. PLoS Pathog 9:e1003545
Marsh EK, van den Berg MCW, May RC (2011) A two-gene balance regulates Salmonella typhimurium tolerance in the nematode Caenorhabditis elegans. PLoS ONE 6:e16839
Meijer K, de Vos P, Priebe MG (2010) Butyrate and other short-chain fatty acids as modulators of immunity: what relevance for health? Curr Opin Clin Nutr Metab Care 13:715–721
Millet ACM, Ewbank JJ (2004) Immunity in Caenorhabditis elegans. Curr Opin Immunol 16:4–9
Mooijaart SP, Brandt BW, Baldal EA, Pijpe J, Kuningas M, Beekman M, Zwaan BJ, Slagboom PE, Westendorp RGJ, Van Heemst D (2005) C. elegans DAF-12, nuclear hormone receptors and human longevity and disease at old age. Ageing Res Rev 4:351–371
Pincus Z, Slack FJ (2010) Developmental biomarkers of aging in Caenorhabditis elegans. Dev Dyn 239:1306–1314
Roberts AF, Gumienny TL, Gleason RJ, Wang H, Padgett RW (2010) Regulation of genes affecting body size and innate immunity by the DBL-1/BMP-like pathway in Caenorhabditis elegans. BMC Dev Biol 10:61
Schmeisser S, Priebe S, Groth M, Monajembashi S, Hemmerich P, Guthke R, Platzer M, Ristow M (2013) Neuronal ROS signaling rather than AMPK/sirtuin-mediated energy sensing links dietary restriction to lifespan extension. Mol Metab 2:92–102
Stiernagle T (1999) Maintenance of C. elegans. In: Hope IA (ed) C. elegans: a practical approach. Oxford University Press, New York, pp 51–59
Wu D, Rea SL, Yashin AI, Johnson TE (2006) Visualizing hidden heterogeneity in isogenic populations of C. elegans. Exp Gerontol 41:261–270
Zhang R, Hou A (2013) Host-microbe interactions in Caenorhabditis elegans. ISRN Microbiol 2013:356451
Zhao L, Zhao Y, Liu R, Zheng X, Zhang M, Guo H, Zhang H, Ren F (2017) The transcription factor DAF-16 is essential for increased longevity in C. elegans exposed to Bifidobacterium longum BB68. Sci Rep 7:7408
Zhao Y, Zhao L, Zheng X, Fu T, Guo H, Ren F (2013) Lactobacillus salivarius strain FDB89 induced longevity in Caenorhabditis elegans by dietary restriction. J Microbiol 51:183–188
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This study was supported by Korea University Grant (K1711191).
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Kwon, G., Lee, J., Koh, JH. et al. Lifespan Extension of Caenorhabditis elegans by Butyricicoccus pullicaecorum and Megasphaera elsdenii with Probiotic Potential. Curr Microbiol 75, 557–564 (2018). https://doi.org/10.1007/s00284-017-1416-6
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DOI: https://doi.org/10.1007/s00284-017-1416-6