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

17Citations
Citations of this article
73Readers
Mendeley users who have this article in their library.

This article is free to access.

Abstract

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. © 2012 Leroy et al.; licensee BioMed Central Ltd.

Figures

  • Figure 1 Survival of C. elegans developed on different E. coli strains. (A) Survival of N2 nematodes to the innocuous E. coli OP50 strain following development on the pathogenic 536 strain (536/OP50 n= 93 and OP50/OP50 n= 90, independent replicates N= 3). There is no difference in nematodes survival despite the difference in developmental condition indicating that development on the pathogenic 536 strain has no deleterious effect on survival. (B) Survival of N2 nematodes to E. coli 536 strain following development on the pathogenic 536 strain (536/536 n= 80 and OP50/536 n= 80, N= 7). N2 nematodes had a significantly greater survival on strain 536 following development on 536 than on OP50 strains. (C) Survival of N2 nematodes to E. faecalis OG1RF strain following development on E. faecalis OG1RF (OG1RF/OG1RF n = 86, OP50/OG1RF n= 81, N= 3). As seen with E. coli 536, development on E. faecalis OG1RF prior to adults exposure to the same strain significantly increases nematodes survival compared to those developed on OP50 strain. (D) Survival of N2 nematodes to E. faecalis OG1RF strain following development on E. coli 536 (536/OG1RF n= 100 and OP50/OG1RF n= 104, N = 3). Development on E. coli 536 significantly increases survival to E. faecalis OG1RF strain in a similar manner as development on E. faecalis OG1RF, and is thus not due to adaptation to one bacterial strain during nematode development. Graphed: ns: not significant, *: p < 0.05, **: p < 0.01, ***: p < 0.001, ****: p < 0.0001.
  • Figure 2 C. elegans signaling pathways involved in developmental modulation of longevity. Survival of C. elegans mutants to E. coli 536 pathogen following development on strains 536 (536/536) or OP50 (OP50/536) and life through OP50 control (OP50/OP50). (A & B) C. elegans daf-16 mutants allele mu86 (536/536 n= 80, OP50/536 n= 80, and OP50/OP50 n= 80, independent repeats N = 4) and mgDf50 (536/536 n = 65, OP50/536 n= 56, and OP50/OP50 n= 61, N = 3), (C) C. elegans dbl-1 mutant (536/536 n= 127, OP50/536 n= 124, and OP50/OP50 n= 88, N = 4), and (D) C. elegans pmk-1 mutant (536/536 n= 80, OP50/536 n= 78, and OP50/OP50 n= 77, N = 8). No differential survival of daf-16 and dbl-1 nematodes to E. coli 536 based on developmental conditions was observed, while a small but statistically significant difference in survival to E. coli 536 strain was observed for C. elegans pmk-1 mutant depending on developmental conditions. Graphed: ns: not significant, *: p < 0.05, **: p < 0.01, ***: p < 0.001, ****: p < 0.0001.
  • Figure 3 Heat-shock resistance and hsp-16.2 induction in C. elegans developed on different E. coli strains. (A) Survival proportion of nematodes developed on OP50 or 536 E. coli strains after a 10 h heat shock at 35°C. Following development on strain 536, 20% more nematodes survived the 10 h heat shock treatment compared to nematodes developed on strain OP50. (B) Level of fluorescence of the hsp-16.2::GFP reporter in young adult nematodes (day 0) developed on E. coli 536 pathogen (n=75) or OP50 strain (n=75). (C) Two day-old adult nematodes exposed to the 536 pathogenic strain had a higher level of induction of hsp-16.2 following development on strain 536 (536/536 n=150) than those developed on strain OP50 (OP50/536 n=88) and those maintained life through on strain OP50 (OP50/OP50 n=98). (D) Quantity of live bacterial cells in the intestinal tract of 2-day old nematodes exposed to E. coli 536 following development on strains 536 (536/536 n=5) or OP50 (OP50/536 n=5) and controls maintained life through on strain OP50 (OP50/OP50 n=5). The observed difference in the level of hsp-16.2 induction cannot be correlated with the amount of live bacteria colonizing the nematode intestinal tracts as there was no significant difference in the mean bacterial density in the intestine of 2-day old nematodes exposed to E. coli 536 independently of whether they were developed on strains OP50 or 536. Graphed: mean ± s.e.m., *: p<0.05, **: p<0.01, ***: p<0.001.

References Powered by Scopus

Pathogenic Escherichia coli

4106Citations
N/AReaders
Get full text

The fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans

1625Citations
N/AReaders
Get full text

How host-microbial interactions shape the nutrient environment of the mammalian intestine

1335Citations
N/AReaders
Get full text

Cited by Powered by Scopus

Oxidative stress and hormesis in evolutionary ecology and physiology: A marriage between mechanistic and evolutionary approaches

273Citations
N/AReaders
Get full text

The C. elegans healthspan and stress-resistance assay toolkit

64Citations
N/AReaders
Get full text

Hormesis results in trade-offs with immunity

38Citations
N/AReaders
Get full text

Register to see more suggestions

Mendeley helps you to discover research relevant for your work.

Already have an account?

Cite

CITATION STYLE

APA

Leroy, M., Mosser, T., Manière, X., Alvarez, D. F., & Matic, I. (2012). Pathogen-induced Caenorhabditis elegans developmental plasticity has a hormetic effect on the resistance to biotic and abiotic stresses. BMC Evolutionary Biology, 12(1). https://doi.org/10.1186/1471-2148-12-187

Readers over time

‘12‘13‘14‘15‘16‘17‘18‘19‘20‘21‘22‘23‘240481216

Readers' Seniority

Tooltip

PhD / Post grad / Masters / Doc 25

56%

Researcher 12

27%

Professor / Associate Prof. 7

16%

Lecturer / Post doc 1

2%

Readers' Discipline

Tooltip

Agricultural and Biological Sciences 39

74%

Biochemistry, Genetics and Molecular Bi... 9

17%

Immunology and Microbiology 4

8%

Philosophy 1

2%

Save time finding and organizing research with Mendeley

Sign up for free
0