Dataset Information

Robustness of the bacterial community in the cabbage white butterfly larval midgut.

ABSTRACT: Microbial communities typically vary in composition and structure over space and time. Little is known about the inherent characteristics of communities that govern various drivers of these changes, such as random variation, changes in response to perturbation, or susceptibility to invasion. In this study, we use 16S ribosomal RNA gene sequences to describe variation among bacterial communities in the midguts of cabbage white butterfly (Pieris rapae) larvae and examine the influence of community structure on susceptibility to invasion. We compared communities in larvae experiencing the same conditions at different times (temporal variation) or fed different diets (perturbation). The most highly represented phylum was Proteobacteria, which was present in all midgut communities. The observed species richness ranged from six to 15, and the most abundant members affiliated with the genera Methylobacteria, Asaia, Acinetobacter, Enterobacter, and Pantoea. Individual larvae subjected to the same conditions at the same time harbored communities that were highly similar in structure and membership, whereas the communities observed within larval populations changed with diet and over time. In addition, structural changes due to perturbation coincided with enhanced susceptibility to invasion by Enterobacter sp. NAB3R and Pantoea stewartii CWB600, suggesting that resistance to invasion is in part governed by community structure. These findings along with the observed conservation of membership at the phylum level, variation in structure and membership at lower taxonomic levels, and its relative simplicity make the cabbage white butterfly larval community an attractive model for studying community dynamics and robustness.

SUBMITTER: Robinson CJ

PROVIDER: S-EPMC2836246 | biostudies-literature | 2010 Feb

REPOSITORIES: biostudies-literature

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Robustness of the bacterial community in the cabbage white butterfly larval midgut.

Robinson Courtney J CJ Schloss Patrick P Ramos Yolied Y Raffa Kenneth K Handelsman Jo J

Microbial ecology 20100201 2

Microbial communities typically vary in composition and structure over space and time. Little is known about the inherent characteristics of communities that govern various drivers of these changes, such as random variation, changes in response to perturbation, or susceptibility to invasion. In this study, we use 16S ribosomal RNA gene sequences to describe variation among bacterial communities in the midguts of cabbage white butterfly (Pieris rapae) larvae and examine the influence of community ...[more]

PMID: 19924467

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Project description:To successfully exert defenses against herbivores and pathogens plants need to recognize reliable cues produced by their attackers. Up to now, few elicitors associated with herbivorous insects have been identified. We have previously shown that accessory reproductive gland secretions associated with eggs of Cabbage White butterflies (Pieris spp.) induce chemical changes in Brussels sprouts plants recruiting egg-killing parasitoids. Only secretions of mated female butterflies contain minute amounts of male-derived anti-aphrodisiac compounds that elicit this indirect plant defense. Here, we used the black mustard (Brassica nigra) to investigate how eggs of the Large Cabbage White butterfly (Pieris brassicae) induce, either an egg-killing direct [i.e., hypersensitive response (HR)-like necrosis] or indirect defense (i.e., oviposition-induced plant volatiles attracting Trichogramma egg parasitoids). Plants induced by P. brassicae egg-associated secretions expressed both traits and previous mating enhanced elicitation. Treatment with the anti-aphrodisiac compound of P. brassicae, benzyl cyanide (BC), induced stronger HR when compared to controls. Expression of the salicylic (SA) pathway- and HR-marker PATHOGENESIS-RELATED GENE1 was induced only in plants showing an HR-like necrosis. Trichogramma wasps were attracted to volatiles induced by secretion of mated P. brassicae females but application of BC did not elicit the parasitoid-attracting volatiles. We conclude that egg-associated secretions of Pieris butterflies contain specific elicitors of the different plant defense traits against eggs in Brassica plants. While in Brussels sprouts plants anti-aphrodisiac compounds in Pieris egg-associated secretions were clearly shown to elicit indirect defense, the wild relative B. nigra, recognizes different herbivore cues that mediate the defensive responses. These results add another level of specificity to the mechanisms by which plants recognize their attackers.

Project description:BackgroundTicks are obligate hematophagous arthropods transmitting a wide range of pathogens to humans and animals. They also harbor a non-pathogenic microbiota, primarily in the ovaries and the midgut. In the previous study on Ixodes ricinus, we used a culture-independent approach and showed a diverse but quantitatively poor midgut bacterial microbiome. Our analysis also revealed the absence of a core microbiome, suggesting an environmental origin of the tick midgut microbiota.MethodsA bacterial analysis of the midgut of adult females collected by flagging from two localities in the Czech Republic was performed. Using the culture-independent approach, we tested the hypothesis that the midgut microbiome is of the environmental origin. We also cultured indigenous bacteria from the tick midgut and used these to feed ticks artificially in an attempt to manipulate the midgut microbiome.ResultsThe midgut showed a very low prevalence and abundance of culturable bacteria, with only 37% of ticks positive for bacteria. The culture-independent approach revealed the presence of Borrelia sp., Spiroplasma sp., Rickettsia sp., Midichloria sp. and various mainly environmental Gram-positive bacterial taxa. The comparison of ticks from two regions revealed that the habitat influenced the midgut bacterial diversity. In addition, the midgut of ticks capillary fed with the indigenous Micrococcus luteus (Gram-positive) and Pantoea sp. (Gram-negative) could not be colonized due to rapid and effective clearance of both bacterial taxa.ConclusionsThe midgut microbiome of I. ricinus is diverse but low in abundance, with the exception of tick-borne pathogens and symbionts. The environment impacts the diversity of the tick midgut microbiome. Ingested extracellular environmental bacteria are rapidly eliminated and are not able to colonize the gut. We hypothesize that bacterial elimination triggered in the midgut of unfed adult females is critical to maintain low microbial levels during blood-feeding.

Dataset Information

Robustness of the bacterial community in the cabbage white butterfly larval midgut.

Publications

Robustness of the bacterial community in the cabbage white butterfly larval midgut.

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