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Open Access Research article

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

Fernando Gomez1, Gabriela C Monsalve2, Vincent Tse35, Ryoichi Saiki136, Emily Weng3, Laura Lee47, Chandra Srinivasan4, Alison R Frand12 and Catherine F Clarke13*

Author Affiliations

1 Molecular Biology Institute, University of California, Los Angeles, CA, 90095, USA

2 Department of Biological Chemistry, University of California, Los Angeles, CA, 90095, USA

3 Department of Chemistry and Biochemistry, University of California, Los Angeles, CA, 90095, USA

4 Department of Chemistry and Biochemistry, California State University, Fullerton, CA, 92834, USA

5 Present address: C3 Jian, Inc, 4503 Glencoe Ave, Marina del Ray, CA, 90292, USA

6 Present address: Funakoshi Co., Ltd, 9-7 Hongo 2-Chome, Bunkyo-Ku, Tokyo, 113-0033, Japan

7 Present address: City Year Los Angeles, 606 South Olive Street, 2nd Floor, Los Angeles, California, 90014, USA

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BMC Microbiology 2012, 12:300  doi:10.1186/1471-2180-12-300

Published: 20 December 2012

Abstract

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.

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