Pathogen-induced Caenorhabditis elegans developmental plasticity has a hormetic effect on the resistance to biotic and abiotic stresses

BMC Evolutionary Biology

Ivan Matic¹  Diana Fernández Alvarez¹  Xavier Manière¹  Thomas Mosser¹  Magali Leroy¹ 

[1] Laboratory of Evolutive, Medical and Molecular Genetics, Inserm U1001, Université Paris Descartes, Sorbonne Paris Cité, Faculté De Médecine Paris Descartes, 156 rue de Vaugirard, Paris, 75730 cedex 15, France

关键词: Pathogens;    Hormesis;    Stress resistance;    Lifespan;    Development;    Caenorhabditis elegans;   

Others  :  1140282
DOI  :  10.1186/1471-2148-12-187

 received in 2012-05-08, accepted in 2012-09-17,  发布年份 2012

【 摘 要 】

Background

Phenotypic plasticity, i.e. the capacity to change the phenotype in response to changes in the environment without alteration of the genotype, is important for coping with unstable environments. In spite of the ample evidence that microorganisms are a major environmental component playing a significant role in eukaryotic organisms health and disease, there is not much information about the effect of microorganism-induced developmental phenotypic plasticity on adult animals’ stress resistance and longevity.

Results

We examined the consequences of development of Caenorhabditis elegans larvae fed with different bacterial strains on stress resistance and lifespan of adult nematodes. Bacterial strains used in this study were either pathogenic or innocuous to nematodes. Exposure to the pathogen during development did not affect larval survival. However, the development of nematodes on the pathogenic bacterial strains increased lifespan of adult nematodes exposed to the same or a different pathogen. A longer nematode lifespan, developed on pathogens and exposed to pathogens as adults, did not result from an enhanced capacity to kill bacteria, but is likely due to an increased tolerance to the damage inflicted by the pathogenic bacteria. We observed that adult nematodes developed on a pathogen induce higher level of expression of the hsp-16.2 gene and have higher resistance to heat shock than nematodes developed on an innocuous strain. Therefore, the increased resistance to pathogens could be, at least partially, due to the early induction of the heat shock response in nematodes developed on pathogens. The lifespan increase is controlled by the DBL-1 transforming growth factor beta-like, DAF-2/DAF-16 insulin-like, and p38 MAP kinase pathways. Therefore, the observed modulation of adult nematode lifespans by developmental exposure to a pathogen is likely a genetically controlled response.

Conclusions

Our study shows that development on pathogens has a hormetic effect on adult nematodes, as it results in increased resistance to different pathogens and to heat shock. Such developmental plasticity of C. elegans nematodes, which are self-fertilizing homozygous animals producing offspring with negligible genetic variation, could increase the probability of survival in changing environments.

【 授权许可】

   
2012 Leroy et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Braendle C, Felix MA: The other side of phenotypic plasticity: a developmental system that generates an invariant phenotype despite environmental variation. J Biosci 2009, 34(4):543-551.
• [2]Gluckman P, Hanson M: Developmental Origins of Health and Disease. Cambridge University Press, Cambridge, UK; 2006.
• [3]Hall SE, Beverly M, Russ C, Nusbaum C, Sengupta P: A cellular memory of developmental history generates phenotypic diversity in C. elegans. Curr Biol 2010, 20(2):149-155.
• [4]Taylor KA, Weinstein PP: The effect of oxygen and carbon dioxide on the development of the free-living stages of Strongyloides ratti in axenic culture. J Parasitol 1990, 76(4):545-551.
• [5]Minato K, Kimura E, Shintoku Y, Uga S: Effect of temperature on the development of free-living stages of Strongyloides ratti. Parasitol Res 2008, 102(2):315-319.
• [6]Gardner MP, Gems D, Viney ME: Extraordinary plasticity in aging in Strongyloides ratti implies a gene-regulatory mechanism of lifespan evolution. Aging Cell 2006, 5(4):315-323.
• [7]Laforsch C, Tollrian R: Embryological aspects of inducible morphological defenses in Daphnia. J Morphol 2004, 262(3):701-707.
• [8]Bakula M: The persistence of a microbial flora during postembryogenesis of Drosophila melanogaster. J Invertebr Pathol 1969, 14(3):365-374.
• [9]Rawls JF, Samuel BS, Gordon JI: Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci USA 2004, 101(13):4596-4601.
• [10]Szewczyk NJ, Udranszky IA, Kozak E, Sunga J, Kim SK, Jacobson LA, Conley CA: Delayed development and lifespan extension as features of metabolic lifestyle alteration in C. elegans under dietary restriction. J Exp Biol 2006, 209(Pt 20):4129-4139.
• [11]Macpherson AJ, Hapfelmeier S, McCoy KD: The armed truce between the intestinal microflora and host mucosal immunity. Semin Immunol 2007, 19(2):57-58.
• [12]Bry L, Falk PG, Midtvedt T, Gordon JI: A model of host-microbial interactions in an open mammalian ecosystem. Science 1996, 273(5280):1380-1383.
• [13]Stappenbeck TS, Hooper LV, Gordon JI: Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci USA 2002, 99(24):15451-15455.
• [14]Hooper LV, Midtvedt T, Gordon JI: How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 2002, 22:283-307.
• [15]Casadevall A, Pirofski LA: Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect Immun 1999, 67(8):3703-3713.
• [16]Brenner S: The genetics of Caenorhabditis elegans. Genetics 1974, 77(1):71-94.
• [17]Sulston J, Hodgkin J: Methods. In The Nematode Caenorhabditis elegans. Edited by Wood WB. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA; 1988:587-606.
• [18]Kaper JB, Nataro JP, Mobley HL: Pathogenic Escherichia coli. Nat Rev Microbiol 2004, 2(2):123-140.
• [19]Diard M, Baeriswyl S, Clermont O, Gouriou S, Picard B, Taddei F, Denamur E, Matic I: Caenorhabditis elegans as a simple model to study phenotypic and genetic virulence determinants of extraintestinal pathogenic Escherichia coli. Microbes Infect 2007, 9(2):214-223.
• [20]Baeriswyl S, Diard M, Mosser T, Leroy M, Maniere X, Taddei F, Matic I: Modulation of aging profiles in isogenic populations of Caenorhabditis elegans by bacteria causing different extrinsic mortality rates. Biogerontology 2010, 11(1):53-65.
• [21]Calabrese EJ, Bachmann KA, Bailer AJ, Bolger PM, Borak J, Cai L, Cedergreen N, Cherian MG, Chiueh CC, Clarkson TW, et al.: Biological stress response terminology: Integrating the concepts of adaptive response and preconditioning stress within a hormetic dose–response framework. Toxicol Appl Pharmacol 2007, 222(1):122-128.
• [22]Mattson MP: Hormesis defined. Ageing Res Rev 2008, 7(1):1-7.
• [23]Johnson JR, Clermont O, Menard M, Kuskowski MA, Picard B, Denamur E: Experimental mouse lethality of Escherichia coli isolates, in relation to accessory traits, phylogenetic group, and ecological source. J Infect Dis 2006, 194(8):1141-1150.
• [24]Diard M, Garry L, Selva M, Mosser T, Denamur E, Matic I: Extra-intestinal pathogenic Escherichia coli pathogenicity associated islands are fitness elements involved in the intestinal colonization. J Bacteriol 2010, 192(19):4885-4893.
• [25]Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA, Ruvkun G: The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 1997, 389(6654):994-999.
• [26]Mochii M, Yoshida S, Morita K, Kohara Y, Ueno N: Identification of transforming growth factor-beta-regulated genes in Caenorhabditis elegans by differential hybridization of arrayed cDNAs. Proc Natl Acad Sci USA 1999, 96(26):15020-15025.
• [27]Partridge FA, Gravato-Nobre MJ, Hodgkin J: Signal transduction pathways that function in both development and innate immunity. Dev Dyn 2010, 239(5):1330-1336.
• [28]Ewbank JJ: Signaling in the immune response. WormBook edition. The C. elegans Research Community, WormBook; 2006:1-12. http://www.wormbook.org webcite
• [29]Ben-Zvi A, Miller EA, Morimoto RI: Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc Natl Acad Sci USA 2009, 106(35):14914-14919.
• [30]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.
• [31]Hsu AL, Murphy CT, Kenyon C: Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 2003, 300(5622):1142-1145.
• [32]Rea SL, Wu D, Cypser JR, Vaupel JW, Johnson TE: A stress-sensitive reporter predicts longevity in isogenic populations of Caenorhabditis elegans. Nat Genet 2005, 37(8):894-898.
• [33]Medzhitov R, Schneider DS, Soares MP: Disease tolerance as a defense strategy. Science 2012, 335(6071):936-941.
• [34]Schulenburg H, Ewbank JJ: The genetics of pathogen avoidance in Caenorhabditis elegans. Mol Microbiol 2007, 66(3):563-570.
• [35]Felix MA, Braendle C: The natural history of Caenorhabditis elegans. Curr Biol 2010, 20(22):R965-969.
• [36]Bargmann CI, Hartwieg E, Horvitz HR: Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 1993, 74(3):515-527.
• [37]Melo JA, Ruvkun G: Inactivation of conserved C. elegans genes engages pathogen- and xenobiotic-associated defenses. Cell 2012, 149(2):452-466.
• [38]O’Halloran DM, Fitzapatrick DA, Burnell MA: The chemosensory system of Caenorhabditis elegans and other nematodes. In Chemical ecology: from gene to ecosystem. Edited by Dicke M, Takken W. Springer-Verlag, Heidelberg, Germany; 2006:71-88.
• [39]Pradel E, Zhang Y, Pujol N, Matsuyama T, Bargmann CI, Ewbank JJ: Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. Proc Natl Acad Sci USA 2007, 104(7):2295-2300.
• [40]Shtonda BB, Avery L: Dietary choice behavior in Caenorhabditis elegans. J Exp Biol 2006, 209(Pt 1):89-102.
• [41]Read AF, Graham AL, Raberg L: Animal defenses against infectious agents: is damage control more important than pathogen control. PLoS Biol 2008, 6(12):e4.
• [42]Hajdu-Cronin YM, Chen WJ, Sternberg PW: The L-type cyclin CYL-1 and the heat-shock-factor HSF-1 are required for heat-shock-induced protein expression in Caenorhabditis elegans. Genetics 2004, 168(4):1937-1949.
• [43]Singh V, Aballay A: Heat shock and genetic activation of HSF-1 enhance immunity to bacteria. Cell Cycle 2006, 5(21):2443-2446.
• [44]Walker GA, Thompson FJ, Brawley A, Scanlon T, Devaney E: Heat shock factor functions at the convergence of the stress response and developmental pathways in Caenorhabditis elegans. FASEB J 2003, 17(13):1960-1962.
• [45]Wu D, Rea SL, Yashin AI, Johnson TE: Visualizing hidden heterogeneity in isogenic populations of C. elegans. Exp Gerontol 2006, 41(3):261-270.
• [46]Fonte V, Kipp DR, Yerg J 3rd, Merin D, Forrestal M, Wagner E, Roberts CM, Link CD: Suppression of in vivo beta-amyloid peptide toxicity by overexpression of the HSP-16.2 small chaperone protein. J Biol Chem 2008, 283(2):784-791.
• [47]Zhou KI, Pincus Z, Slack FJ: Longevity and stress in Caenorhabditis elegans. Aging (Albany NY) 2011, 3(8):733-753.
• [48]Garsin DA, Villanueva JM, Begun J, Kim DH, Sifri CD, Calderwood SB, Ruvkun G, Ausubel FM: Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 2003, 300(5627):1921.
• [49]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
• [50]Cypser JR, Tedesco P, Johnson TE: Hormesis and aging in Caenorhabditis elegans. Exp Gerontol 2006, 41(10):935-939.
• [51]Cypser JR, Johnson TE: Multiple stressors in Caenorhabditis elegans induce stress hormesis and extended longevity. J Gerontol A Biol Sci Med Sci 2002, 57(3):B109-114.
• [52]Anyanful A, Easley KA, Benian GM, Kalman D: Conditioning protects C. elegans from lethal effects of enteropathogenic E. coli by activating genes that regulate lifespan and innate immunity. Cell Host Microbe 2009, 5(5):450-462.
• [53]Kim Y, Mylonakis E: Caenorhabditis elegans immune conditioning with the probiotic bacterium Lactobacillus acidophilus strain NCFM enhances gram-positive immune responses. Infect Immun 2012, 80(7):2500-2508.
• [54]Sadd BM, Schmid-Hempel P: Insect immunity shows specificity in protection upon secondary pathogen exposure. Curr Biol 2006, 16(12):1206-1210.
• [55]Moret Y: “Trans-generational immune priming”: specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc Biol Sci 2006, 273(1592):1399-1405.
• [56]Brummel T, Ching A, Seroude L, Simon AF, Benzer S: Drosophila lifespan enhancement by exogenous bacteria. Proc Natl Acad Sci USA 2004, 101(35):12974-12979.
• [57]von Mutius E, Braun-Fahrlander C, Schierl R, Riedler J, Ehlermann S, Maisch S, Waser M, Nowak D: Exposure to endotoxin or other bacterial components might protect against the development of atopy. Clin Exp Allergy 2000, 30(9):1230-1234.
• [58]Adlerberth I, Lindberg E, Aberg N, Hesselmar B, Saalman R, Strannegard IL, Wold AE: Reduced enterobacterial and increased staphylococcal colonization of the infantile bowel: an effect of hygienic lifestyle? Pediatr Res 2006, 59(1):96-101.
• [59]Riedler J, Braun-Fahrlander C, Eder W, Schreuer M, Waser M, Maisch S, Carr D, Schierl R, Nowak D, von Mutius E: Exposure to farming in early life and development of asthma and allergy: a cross-sectional survey. Lancet 2001, 358(9288):1129-1133.
• [60]Wold AE: The hygiene hypothesis revised: is the rising frequency of allergy due to changes in the intestinal flora? Allergy 1998, 53(46 Suppl):20-25.
• [61]Lucas A: Programming by early nutrition: an experimental approach. J Nutr 1998, 128(2 Suppl):401S-406S.
• [62]Mitchell A, Romano GH, Groisman B, Yona A, Dekel E, Kupiec M, Dahan O, Pilpel Y: Adaptive prediction of environmental changes by microorganisms. Nature 2009, 460(7252):220-224.
• [63]Dunny GM, Brown BL, Clewell DB: Induced cell aggregation and mating in Streptococcus faecalis: evidence for a bacterial sex pheromone. Proc Natl Acad Sci USA 1978, 75(7):3479-3483.
• [64]Pujol N, Link EM, Liu LX, Kurz CL, Alloing G, Tan MW, Ray KP, Solari R, Johnson CD, Ewbank JJ: A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr Biol 2001, 11(11):809-821.