Delayed accumulation of intestinal coliform bacteria enhances life span and stress resistance in Caenorhabditis elegans fed respiratory deficient E. coli

BMC Microbiology

Catherine F Clarke⁴  Alison R Frand⁵  Chandra Srinivasan¹  Laura Lee⁷  Emily Weng⁴  Ryoichi Saiki³  Vincent Tse²  Gabriela C Monsalve⁵  Fernando Gomez⁶ 

[1] Department of Chemistry and Biochemistry, California State University, Fullerton, CA, 92834, USA;Present address: C3 Jian, Inc, 4503 Glencoe Ave, Marina del Ray, CA, 90292, USA;Present address: Funakoshi Co., Ltd, 9-7 Hongo 2-Chome, Bunkyo-Ku, Tokyo, 113-0033, Japan;Department of Chemistry and Biochemistry, University of California, Los Angeles, CA, 90095, USA;Department of Biological Chemistry, University of California, Los Angeles, CA, 90095, USA;Molecular Biology Institute, University of California, Los Angeles, CA, 90095, USA;Present address: City Year Los Angeles, 606 South Olive Street, 2nd Floor, Los Angeles, California, 90014, USA

关键词: Respiration;    Probiotic;    Pharynx;    Life span;    Intestine;    Gut microbiome;    Coenzyme Q;    Bacterial colonization;    Aging;   

Others  :  1144671
DOI  :  10.1186/1471-2180-12-300

 received in 2012-08-01, accepted in 2012-12-14,  发布年份 2012

【 摘 要 】

Background

Studies with the nematode model Caenorhabditis elegans have identified conserved biochemical pathways that act to modulate life span. Life span can also be influenced by the composition of the intestinal microbiome, and C. elegans life span can be dramatically influenced by its diet of Escherichia coli. Although C. elegans is typically fed the standard OP50 strain of E. coli, nematodes fed E. coli strains rendered respiratory deficient, either due to a lack coenzyme Q or the absence of ATP synthase, show significant life span extension. Here we explore the mechanisms accounting for the enhanced nematode life span in response to these diets.

Results

The intestinal load of E. coli was monitored by determination of worm-associated colony forming units (cfu/worm or coliform counts) as a function of age. The presence of GFP-expressing E. coli in the worm intestine was also monitored by fluorescence microscopy. Worms fed the standard OP50 E. coli strain have high cfu and GFP-labeled bacteria in their guts at the L4 larval stage, and show saturated coliform counts by day five of adulthood. In contrast, nematodes fed diets of respiratory deficient E. coli lacking coenzyme Q lived significantly longer and failed to accumulate bacteria within the lumen at early ages. Animals fed bacteria deficient in complex V showed intermediate coliform numbers and were not quite as long-lived. The results indicate that respiratory deficient Q-less E. coli are effectively degraded in the early adult worm, either at the pharynx or within the intestine, and do not accumulate in the intestinal tract until day ten of adulthood.

Conclusions

The findings of this study suggest that the nematodes fed the respiratory deficient E. coli diet live longer because the delay in bacterial colonization of the gut subjects the worms to less stress compared to worms fed the OP50 E. coli diet. This work suggests that bacterial respiration can act as a virulence factor, influencing the ability of bacteria to colonize and subsequently harm the animal host. Respiratory deficient bacteria may pose a useful model for probing probiotic relationships within the gut microbiome in higher organisms.

【 授权许可】

   
2012 Gomez et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

【 参考文献 】

• [1]Prakash S, Rodes L, Coussa-Charley M, Tomaro-Duchesneau C: Gut microbiota: next frontier in understanding human health and development of biotherapeutics. Biologics: targets & therapy 2011, 5:71-86.
• [2]Mai V, Draganov PV: Recent advances and remaining gaps in our knowledge of associations between gut microbiota and human health. World J Gastroenterol 2009, 15(1):81-85.
• [3]Dobrogosz WJ, Peacock TJ, Hassan HM: Evolution of the probiotic concept from conception to validation and acceptance in medical science. Adv Appl Microbiol 2010, 72:1-41.
• [4]Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA: Diversity of the human intestinal microbial flora. Science 2005, 308(5728):1635-1638.
• [5]Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al.: Human gut microbiome viewed across age and geography. Nature 2012, 486(7402):222-227.
• [6]Gill HS, Rutherfurd KJ, Cross ML, Gopal PK: Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobacterium lactis HN019. Am J Clin Nutr 2001, 74(6):833-839.
• [7]Ottaviani E, Ventura N, Mandrioli M, Candela M, Franchini A, Franceschi C: Gut microbiota as a candidate for lifespan extension: an ecological/evolutionary perspective targeted on living organisms as metaorganisms. Biogerontology 2011, 12(6):599-609.
• [8]Bhathena J, Martoni C, Kulamarva A, Urbanska AM, Malhotra M, Prakash S: Orally delivered microencapsulated live probiotic formulation lowers serum lipids in hypercholesterolemic hamsters. J Med Food 2009, 12(2):310-319.
• [9]Matsumoto M, Kurihara S, Kibe R, Ashida H, Benno Y: Longevity in mice is promoted by probiotic-induced suppression of colonic senescence dependent on upregulation of gut bacterial polyamine production. PLoS One 2011, 6(8):e23652.
• [10]Wilkinson DS, Taylor RC, Dillin A: Analysis of aging in Caenorhabditis elegans. Methods Cell Biol 2012, 107:353-381.
• [11]Collins JJ, Huang C, Hughes S, Kornfeld K: The measurement and analysis of age-related changes in Caenorhabditis elegans. The C. elegans Research Community, WormBook; 2007. http://www.wormbook.org webcite
• [12]Herndon LA, Schmeissner PJ, Dudaronek JM, Brown PA, Listner KM, Sakano Y, Paupard MC, Hall DH, Driscoll M: Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 2002, 419(6909):808-814.
• [13]Chow DK, Glenn CF, Johnston JL, Goldberg IG, Wolkow CA: Sarcopenia in the Caenorhabditis elegans pharynx correlates with muscle contraction rate over lifespan. Exp Gerontol 2006, 41(3):252-260.
• [14]Garigan D, Hsu AL, Fraser AG, Kamath RS, Ahringer J, Kenyon C: Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation. Genetics 2002, 161(3):1101-1112.
• [15]McGee MD, Weber D, Day N, Vitelli C, Crippen D, Herndon LA, Hall DH, Melov S: Loss of intestinal nuclei and intestinal integrity in aging C. elegans. Aging Cell 2011, 10(4):699-710.
• [16]Ikeda T, Yasui C, Hoshino K, Arikawa K, Nishikawa Y: Influence of lactic acid bacteria on longevity of Caenorhabditis elegans and host defense against Salmonella enterica serovar enteritidis. Appl Environ Microbiol 2007, 73(20):6404-6409.
• [17]Larsen PL, Clarke CF: Extension of life span in C. elegans by a diet lacking coenzyme Q. Science 2002, 295:120-123.
• [18]Saiki R, Lunceford AL, Bixler T, Dang P, Lee W, Furukawa S, Larsen PL, Clarke CF: Altered bacterial metabolism, not coenzyme Q content, is responsible for the lifespan extension in Caenorhabditis elegans fed an Escherichia coli diet lacking coenzyme Q. Aging Cell 2008, 7(3):291-304.
• [19]Darby C: Interactions with microbial pathogens. The C. elegans Research Community, WormBook; 2005. http://www.wormbook.org webcite
• [20]Gomez F, Saiki R, Chin R, Srinivasan C, Clarke CF: Restoring de novo coenzyme Q biosynthesis in Caenorhabditis elegans coq-3 mutants yields profound rescue compared to exogenous coenzyme Q supplementation. Gene 2012, 506:106-116.
• [21]Bishop NA, Guarente L: Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature 2007, 447(7144):545-549.
• [22]Sykiotis GP, Habeos IG, Samuelson AV, Bohmann D: The role of the antioxidant and longevity-promoting Nrf2 pathway in metabolic regulation. Curr Opin Clin Nutr Metab Care 2011, 14(1):41-48.
• [23]Jonassen T, Larsen PL, Clarke CF: A dietary source of coenzyme Q is essential for growth of long-lived Caenorhabditis elegans clk-1 mutants. Proc Natl Acad Sci U S A 2001, 98:421-426.
• [24]Miyadera H, Amino H, Hiraishi A, Taka H, Murayama K, Miyoshi H, Sakamoto K, Ishii N, Hekimi S, Kita K: Altered quinone biosynthesis in the long-lived clk-1 mutants of Caenorhabditis elegans. J Biol Chem 2001, 276(11):7713-7716.
• [25]Jonassen T, Clarke CF: Isolation and functional expression of human COQ3, a gene encoding a methyltransferase required for ubiquinone biosynthesis. J Biol Chem 2000, 275:12381-12387.
• [26]Hihi AK, Gao Y, Hekimi S: Ubiquinone is necessary for Caenorhabditis elegans development at mitochondrial and non-mitochondrial sites. J Biol Chem 2002, 277(3):2202-2206.
• [27]Khare S, Gomez T, Linster CL, Clarke SG: Defective responses to oxidative stress in protein l-isoaspartyl repair-deficient Caenorhabditis elegans. Mech Ageing Dev 2009, 130(10):670-680.
• [28]Hasegawa K, Miwa S, Tsutsumiuchi K, Miwa J: Allyl isothiocyanate that induces GST and UGT expression confers oxidative stress resistance on C. elegans, as demonstrated by nematode biosensor. PLoS One 2010, 5(2):e9267.
• [29]de Castro E, de Hegi Castro S, Johnson TE: Isolation of long-lived mutants in Caenorhabditis elegans using selection for resistance to juglone. Free Radic Biol Med 2004, 37(2):139-145.
• [30]Becker S, Vlad D, Schuster S, Pfeiffer P, Unden G: Regulatory O2 tensions for the synthesis of fermentation products in Escherichia coli and relation to aerobic respiration. Arch Microbiol 1997, 168(4):290-296.
• [31]Gonidakis S, Finkel SE, Longo VD: Lifespan extension and paraquat resistance in a ubiquinone-deficient Escherichia coli mutant depend on transcription factors ArcA and TdcA. Aging 2011, 3(3):291-303.
• [32]Portal-Celhay C, Bradley ER, Blaser MJ: Control of intestinal bacterial proliferation in regulation of lifespan in Caenorhabditis elegans. BMC Microbiol 2012, 12:49. BioMed Central Full Text
• [33]Butlin JD, Cox GB, Gibson F: Oxidative phosphorylation in Escherichia coli K12. Mutations affecting magnesium ion- or calcium ion-stimulated adenosine triphosphatase. Biochem J 1971, 124(1):75-81.
• [34]Labrousse A, Chauvet S, Couillault C, Kurz CL, Ewbank JJ: Caenorhabditis elegans is a model host for Salmonella typhimurium. Curr Biol 2000, 10(23):1543-1545.
• [35]Kurz CL, Chauvet S, Andres E, Aurouze M, Vallet I, Michel GP, Uh M, Celli J, Filloux A, De Bentzmann S, et al.: Virulence factors of the human opportunistic pathogen Serratia marcescens identified by in vivo screening. EMBO J 2003, 22(7):1451-1460.
• [36]Hill S, Hirano K, Shmanai VV, Marbois BN, Vidovic D, Bekish AV, Kay B, Tse V, Fine J, Clarke CF, et al.: Isotope-reinforced polyunsaturated fatty acids protect yeast cells from oxidative stress. Free Radic Biol Med 2010, 50:130-138.
• [37]Gems D, Riddle DL: Genetic, behavioral and environmental determinants of male longevity in Caenorhabditis elegans. Genetics 2000, 154(4):1597-1610.
• [38]Garsin DA, Sifri CD, Mylonakis E, Qin X, Singh KV, Murray BE, Calderwood SB, Ausubel FM: A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci U S A 2001, 98(19):10892-10897.
• [39]Aballay A, Yorgey P, Ausubel FM: Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr Biol 2000, 10(23):1539-1542.
• [40]Hahm JH, Kim S, Paik YK: GPA-9 is a novel regulator of innate immunity against Escherichia coli foods in adult Caenorhabditis elegans. Aging Cell 2011, 10(2):208-219.
• [41]Marteyn B, Scorza FB, Sansonetti PJ, Tang C: Breathing life into pathogens: the influence of oxygen on bacterial virulence and host responses in the gastrointestinal tract. Cell Microbiol 2011, 13(2):171-176.
• [42]Bekker M, Alexeeva S, Laan W, Sawers G, de Teixeira Mattos J, Hellingwerf K: The ArcBA two-component system of Escherichia coli is regulated by the redox state of both the ubiquinone and the menaquinone pool. J Bacteriol 2010, 192(3):746-754.
• [43]Sengupta N, Paul K, Chowdhury R: The global regulator ArcA modulates expression of virulence factors in Vibrio cholerae. Infect Immun 2003, 71(10):5583-5589.
• [44]Boulette ML, Payne SM: Anaerobic regulation of Shigella flexneri virulence: ArcA regulates Fur and iron acquisition genes. J Bacteriol 2007, 189(19):6957-6967.
• [45]Way SS, Borczuk AC, Goldberg MB: Adaptive immune response to Shigella flexneri 2a cydC in immunocompetent mice and mice lacking immunoglobulin A. Infect Immun 1999, 67(4):2001-2004.
• [46]Endley S, McMurray D, Ficht TA: Interruption of the cydB locus in Brucella abortus attenuates intracellular survival and virulence in the mouse model of infection. J Bacteriol 2001, 183(8):2454-2462.
• [47]Law RJ, Hamlin JN, Sivro A, McCorrister SJ, Cardama GA, Cardona ST: A functional phenylacetic acid catabolic pathway is required for full pathogenicity of Burkholderia cenocepacia in the Caenorhabditis elegans host model. J Bacteriol 2008, 190(21):7209-7218.
• [48]Bae T, Banger AK, Wallace A, Glass EM, Aslund F, Schneewind O, Missiakas DM: Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing. Proc Natl Acad Sci U S A 2004, 101(33):12312-12317.
• [49]Lee H, Yoon H, Ji Y, Kim H, Park H, Lee J, Shin H, Holzapfel W: Functional properties of Lactobacillus strains isolated from kimchi. Int J Food Microbiol 2011, 145(1):155-161.
• [50]Tarmy EM, Kaplan NO: Chemical characterization of D-lactate dehydrogenase from Escherichia coli B. J Biol Chem 1968, 243(10):2579-2586.
• [51]Tsoi SC, Li SS: The nucleotide and deduced amino-acid sequences of a cDNA encoding lactate dehydrogenase from Caenorhabditis elegans: the evolutionary relationships of lactate dehydrogenases from mammals, birds, amphibian, fish, nematode, plants, bacteria, mycoplasma, and plasmodium. Biochem Biophys Res Commun 1994, 205(1):558-564.
• [52]Mshvildadze M, Neu J: Probiotics and prevention of necrotizing enterocolitis. Early Hum Dev 2009, 85(10 Suppl):S71-S74.
• [53]Brady LJ, Gallaher DD, Busta FF: The role of probiotic cultures in the prevention of colon cancer. J Nutr 2000, 130(2S Suppl):410S-414S.
• [54]Shin SC, Kim SH, You H, Kim B, Kim AC, Lee KA, Yoon JH, Ryu JH, Lee WJ: Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 2011, 334(6056):670-674.
• [55]Virk B, Correia G, Dixon DP, Feyst I, Jia J, Oberleitner N, Briggs Z, Hodge E, Edwards R, Ward J, et al.: Excessive folate synthesis limits lifespan in the C. elegans: E. coli aging model. BMC Biol 2012, 10:67. BioMed Central Full Text
• [56]Brenner S: The genetics of Caenorhabditis elegans. Genetics 1974, 77(1):71-94.
• [57]Hsu AY, Poon WW, Shepherd JA, Myles DC, Clarke CF: Complementation of coq3 mutant yeast by mitochondrial targeting of the Escherichia coli UbiG polypeptide: evidence that UbiG catalyzes both O-methylation steps in ubiquinone biosynthesis. Biochemistry 1996, 35(30):9797-9806.