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Bacterial gut symbionts contribute to seed digestion in an omnivorous beetle.

Lundgren JG, Lehman RM - PLoS ONE (2010)

Bottom Line: Bacterial communities of the host varied among the diet and antibiotic treatments.Antibiotics reduced and altered the bacterial communities found in the beetle guts.We conclude that the relationships between the bacterium E. faecalis and this factultative granivore's ability to consume seeds merit further investigation, and that facultative associations with symbiotic bacteria have important implications for the nutritional ecology of their hosts.

View Article: PubMed Central - PubMed

Affiliation: North Central Agricultural Research Laboratory, United States Department of Agriculture-Agricultural Research Service, Brookings, South Dakota, USA. Jonathan.Lundgren@ars.usda.gov

ABSTRACT

Background: Obligate bacterial symbionts alter the diets of host animals in numerous ways, but the ecological roles of facultative bacterial residents that colonize insect guts remain unclear. Carabid beetles are a common group of beneficial insects appreciated for their ability to consume insect prey and seeds, but the contributions of microbes to diet diversification in this and similar groups of facultative granivores are largely unknown.

Methodology and principal findings: Using 16S rRNA gene clone libraries and terminal restriction fragment (tRF) length polymorphism analyses of these genes, we examined the bacterial communities within the guts of facultatively granivorous, adult Harpalus pensylvanicus (Carabidae), fed one of five dietary treatments: 1) an untreated Field population, 2) Seeds with antibiotics (seeds were from Chenopodium album), 3) Seeds without antibiotics, 4) Prey with antibiotics (prey were Acheta domesticus eggs), and 5) Prey without antibiotics. The number of seeds and prey consumed by each beetle were recorded following treatment. Harpalus pensylvanicus possessed a fairly simple gut community of approximately 3-4 bacterial operational taxonomic units (OTU) per beetle that were affiliated with the Gammaproteobacteria, Bacilli, Alphaproteobacteria, and Mollicutes. Bacterial communities of the host varied among the diet and antibiotic treatments. The field population and beetles fed seeds without antibiotics had the closest matching bacterial communities, and the communities in the beetles fed antibiotics were more closely related to each other than to those of the beetles that did not receive antibiotics. Antibiotics reduced and altered the bacterial communities found in the beetle guts. Moreover, beetles fed antibiotics ate fewer seeds, and those beetles that harbored the bacterium Enterococcus faecalis consumed more seeds on average than those lacking this symbiont.

Conclusions/significance: We conclude that the relationships between the bacterium E. faecalis and this factultative granivore's ability to consume seeds merit further investigation, and that facultative associations with symbiotic bacteria have important implications for the nutritional ecology of their hosts.

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The effect of antibiotic treatment on mean (SEM) food consumption by Harpalus pensylvanicus.Beetles were fed prey (eggs of Acheta domesticus) or seeds (Chenopodium album) after being treated with a dietary source of antibiotics for 10 d. An asterisk indicates significant differences between log-transformed means within a food category (α = 0.05).
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pone-0010831-g003: The effect of antibiotic treatment on mean (SEM) food consumption by Harpalus pensylvanicus.Beetles were fed prey (eggs of Acheta domesticus) or seeds (Chenopodium album) after being treated with a dietary source of antibiotics for 10 d. An asterisk indicates significant differences between log-transformed means within a food category (α = 0.05).

Mentions: There was no effect of antibiotics on H. pensylvanicus' consumption of prey (F1, 34 = 1.27, P = 0.27), but consumption of antibiotics was associated with a 40% reduction in seed consumption (F1, 26 = 7.29, P = 0.01; Fig. 3). The reduction in seed consumption was only observed in males (mean ± SEM seed consumption: symbiotic ♂♂, 39.7±8.55 [n = 10]; aposymbiotic ♂♂, 18.29±4.69 [n = 7]; F1, 15 = 4.03, P = 0.06), but not in females (symbiotic ♀♀, 24.83±5.79 [n = 6]; aposymbiotic ♀♀, 21.00±10.33 [n = 6]; F1, 10 = 0.43, P = 0.52). A significant stepwise GLM was created to describe the relationship between bacterial presence/absence and seed consumption in the symbiotic beetles (regression: F2, 13 = 15.04; P<0.001; r2 = 0.70). Only two bacterial tRFs (535 & 903) in the symbiotic treatment were statistically correlated with seed consumption to be included in the stepwise GLM, those beetles with 903 were positively and those with 535 were negatively associated with seed consumption (constant: t = 18.13, P<0.001; 535: t = −4.26, P = 0.001; 903: t = 2.66, P = 0.02). tRF 903 corresponds to the cloned bacterial sequence which most closely matches Enterococcus faecalis R090 (Table 1), which was totally removed from populations fed antibiotics (Fig. 2). Beetles that possessed E. faecalis consumed a mean (SEM) of 56.40±12.41 seeds per beetle, and those without E. faecalis consumed 22.63±3.47 seeds. This bacterial tRF was found in 64.71% of Prey-fed (symbiotic) beetles, 31.25% of Seed-fed (symbiotic) beetles, and 10% of the Field population. Only males in the Seed-fed (symbiotic) and Field populations harbored E. faecalis, whereas eight of 11 beetles in the Prey-fed (symbiotic) that had E. faecalis were females. Only one symbiotic beetle was found to possess tRF 535, and this insect only consumed two seeds. This tRF was not identified in the clone libraries, and occurred exclusively in the symbiotic treatments (including the Field treatment) (Fig. 2).


Bacterial gut symbionts contribute to seed digestion in an omnivorous beetle.

Lundgren JG, Lehman RM - PLoS ONE (2010)

The effect of antibiotic treatment on mean (SEM) food consumption by Harpalus pensylvanicus.Beetles were fed prey (eggs of Acheta domesticus) or seeds (Chenopodium album) after being treated with a dietary source of antibiotics for 10 d. An asterisk indicates significant differences between log-transformed means within a food category (α = 0.05).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2877093&req=5

pone-0010831-g003: The effect of antibiotic treatment on mean (SEM) food consumption by Harpalus pensylvanicus.Beetles were fed prey (eggs of Acheta domesticus) or seeds (Chenopodium album) after being treated with a dietary source of antibiotics for 10 d. An asterisk indicates significant differences between log-transformed means within a food category (α = 0.05).
Mentions: There was no effect of antibiotics on H. pensylvanicus' consumption of prey (F1, 34 = 1.27, P = 0.27), but consumption of antibiotics was associated with a 40% reduction in seed consumption (F1, 26 = 7.29, P = 0.01; Fig. 3). The reduction in seed consumption was only observed in males (mean ± SEM seed consumption: symbiotic ♂♂, 39.7±8.55 [n = 10]; aposymbiotic ♂♂, 18.29±4.69 [n = 7]; F1, 15 = 4.03, P = 0.06), but not in females (symbiotic ♀♀, 24.83±5.79 [n = 6]; aposymbiotic ♀♀, 21.00±10.33 [n = 6]; F1, 10 = 0.43, P = 0.52). A significant stepwise GLM was created to describe the relationship between bacterial presence/absence and seed consumption in the symbiotic beetles (regression: F2, 13 = 15.04; P<0.001; r2 = 0.70). Only two bacterial tRFs (535 & 903) in the symbiotic treatment were statistically correlated with seed consumption to be included in the stepwise GLM, those beetles with 903 were positively and those with 535 were negatively associated with seed consumption (constant: t = 18.13, P<0.001; 535: t = −4.26, P = 0.001; 903: t = 2.66, P = 0.02). tRF 903 corresponds to the cloned bacterial sequence which most closely matches Enterococcus faecalis R090 (Table 1), which was totally removed from populations fed antibiotics (Fig. 2). Beetles that possessed E. faecalis consumed a mean (SEM) of 56.40±12.41 seeds per beetle, and those without E. faecalis consumed 22.63±3.47 seeds. This bacterial tRF was found in 64.71% of Prey-fed (symbiotic) beetles, 31.25% of Seed-fed (symbiotic) beetles, and 10% of the Field population. Only males in the Seed-fed (symbiotic) and Field populations harbored E. faecalis, whereas eight of 11 beetles in the Prey-fed (symbiotic) that had E. faecalis were females. Only one symbiotic beetle was found to possess tRF 535, and this insect only consumed two seeds. This tRF was not identified in the clone libraries, and occurred exclusively in the symbiotic treatments (including the Field treatment) (Fig. 2).

Bottom Line: Bacterial communities of the host varied among the diet and antibiotic treatments.Antibiotics reduced and altered the bacterial communities found in the beetle guts.We conclude that the relationships between the bacterium E. faecalis and this factultative granivore's ability to consume seeds merit further investigation, and that facultative associations with symbiotic bacteria have important implications for the nutritional ecology of their hosts.

View Article: PubMed Central - PubMed

Affiliation: North Central Agricultural Research Laboratory, United States Department of Agriculture-Agricultural Research Service, Brookings, South Dakota, USA. Jonathan.Lundgren@ars.usda.gov

ABSTRACT

Background: Obligate bacterial symbionts alter the diets of host animals in numerous ways, but the ecological roles of facultative bacterial residents that colonize insect guts remain unclear. Carabid beetles are a common group of beneficial insects appreciated for their ability to consume insect prey and seeds, but the contributions of microbes to diet diversification in this and similar groups of facultative granivores are largely unknown.

Methodology and principal findings: Using 16S rRNA gene clone libraries and terminal restriction fragment (tRF) length polymorphism analyses of these genes, we examined the bacterial communities within the guts of facultatively granivorous, adult Harpalus pensylvanicus (Carabidae), fed one of five dietary treatments: 1) an untreated Field population, 2) Seeds with antibiotics (seeds were from Chenopodium album), 3) Seeds without antibiotics, 4) Prey with antibiotics (prey were Acheta domesticus eggs), and 5) Prey without antibiotics. The number of seeds and prey consumed by each beetle were recorded following treatment. Harpalus pensylvanicus possessed a fairly simple gut community of approximately 3-4 bacterial operational taxonomic units (OTU) per beetle that were affiliated with the Gammaproteobacteria, Bacilli, Alphaproteobacteria, and Mollicutes. Bacterial communities of the host varied among the diet and antibiotic treatments. The field population and beetles fed seeds without antibiotics had the closest matching bacterial communities, and the communities in the beetles fed antibiotics were more closely related to each other than to those of the beetles that did not receive antibiotics. Antibiotics reduced and altered the bacterial communities found in the beetle guts. Moreover, beetles fed antibiotics ate fewer seeds, and those beetles that harbored the bacterium Enterococcus faecalis consumed more seeds on average than those lacking this symbiont.

Conclusions/significance: We conclude that the relationships between the bacterium E. faecalis and this factultative granivore's ability to consume seeds merit further investigation, and that facultative associations with symbiotic bacteria have important implications for the nutritional ecology of their hosts.

Show MeSH
Related in: MedlinePlus