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DNA sequencing reveals the midgut microbiota of diamondback moth, Plutella xylostella (L.) and a possible relationship with insecticide resistance.

Xia X, Zheng D, Zhong H, Qin B, Gurr GM, Vasseur L, Lin H, Bai J, He W, You M - PLoS ONE (2013)

Bottom Line: Both insecticide-resistant lines had more Lactobacillales and the much scarcer taxa Pseudomonadales and Xanthomonadales with fewer Enterobacteriales compared with the susceptible strain.While this is consistent with the hypothesis that Lactobacillales or other scarcer taxa play a role in conferring DBM insecticide resistance, further studies are necessary to rule out other possibilities.Findings constitute the basis for future molecular work on the functions of insect midgut microbiota taxa and their possible role in conferring host resistance to toxins.

View Article: PubMed Central - PubMed

Affiliation: Institute of Applied Ecology, Fujian Agriculture and Forestry University, Fuzhou, China.

ABSTRACT

Background: Insect midgut microbiota is important in host nutrition, development and immune response. Recent studies indicate possible links between insect gut microbiota and resistance to biological and chemical toxins. Studies of this phenomenon and symbionts in general have been hampered by difficulties in culture-based approach. In the present study, DNA sequencing was used to examine the midgut microbiota of diamondback moth (DBM), Plutella xylostella (L.), a destructive pest that attacks cruciferous crops worldwide. Its ability to develop resistance to many types of synthetic insecticide and even Bacillus thuringiensis toxins makes it an important species to study.

Methodology/principal findings: Bacteria of the DBM larval midgut in a susceptible and two insecticide (chlorpyrifos and fipronil) resistant lines were examined by Illumina sequencing sampled from an insect generation that was not exposed to insecticide. This revealed that more than 97% of the bacteria were from three orders: Enterobacteriales, Vibrionales and Lactobacillales. Both insecticide-resistant lines had more Lactobacillales and the much scarcer taxa Pseudomonadales and Xanthomonadales with fewer Enterobacteriales compared with the susceptible strain. Consistent with this, a second study observed an increase in the proportion of Lactobacillales in the midgut of DBM individuals from a generation treated with insecticides.

Conclusions/significance: This is the first report of high-throughput DNA sequencing of the entire microbiota of DBM. It reveals differences related to inter- and intra-generational exposure to insecticides. Differences in the midgut microbiota among susceptible and insecticide-resistant lines are independent of insecticide exposure in the sampled generations. While this is consistent with the hypothesis that Lactobacillales or other scarcer taxa play a role in conferring DBM insecticide resistance, further studies are necessary to rule out other possibilities. Findings constitute the basis for future molecular work on the functions of insect midgut microbiota taxa and their possible role in conferring host resistance to toxins.

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Related in: MedlinePlus

Proportional composition of microbes in the DBM larval midgut for the susceptible strain (SS), chlorpyrifos-resistant line (CRL), and fipronil-resistant line (FRL) not exposed to insecticides.(A) Composition at the phylum level, and (B) composition at the order level.
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pone-0068852-g002: Proportional composition of microbes in the DBM larval midgut for the susceptible strain (SS), chlorpyrifos-resistant line (CRL), and fipronil-resistant line (FRL) not exposed to insecticides.(A) Composition at the phylum level, and (B) composition at the order level.

Mentions: Two phyla of bacteria (Firmicutes and Proteobacteria) that were dominant in the midgut of the SS strain were also present in the midgut of both insecticide-resistant lines (CRL and FRL), but their proportions were markedly different (Figure 2A). The frequencies of Firmicutes increased (from 29.52% in SS to 54.79% in CRL and 48.56% in FRL) while frequencies of Proteobacteria decreased (from 70.4% in SS to 45.13% in CRL and 51.05% in FRL). These differences were also marked in the qPCR validation experiment with the insecticide-resistant lines exhibiting a higher proportion of bacteria from the phylum of Firmicutes and a lower proportion of Proteobacteria than the SS strain (Figure S4).


DNA sequencing reveals the midgut microbiota of diamondback moth, Plutella xylostella (L.) and a possible relationship with insecticide resistance.

Xia X, Zheng D, Zhong H, Qin B, Gurr GM, Vasseur L, Lin H, Bai J, He W, You M - PLoS ONE (2013)

Proportional composition of microbes in the DBM larval midgut for the susceptible strain (SS), chlorpyrifos-resistant line (CRL), and fipronil-resistant line (FRL) not exposed to insecticides.(A) Composition at the phylum level, and (B) composition at the order level.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3716819&req=5

pone-0068852-g002: Proportional composition of microbes in the DBM larval midgut for the susceptible strain (SS), chlorpyrifos-resistant line (CRL), and fipronil-resistant line (FRL) not exposed to insecticides.(A) Composition at the phylum level, and (B) composition at the order level.
Mentions: Two phyla of bacteria (Firmicutes and Proteobacteria) that were dominant in the midgut of the SS strain were also present in the midgut of both insecticide-resistant lines (CRL and FRL), but their proportions were markedly different (Figure 2A). The frequencies of Firmicutes increased (from 29.52% in SS to 54.79% in CRL and 48.56% in FRL) while frequencies of Proteobacteria decreased (from 70.4% in SS to 45.13% in CRL and 51.05% in FRL). These differences were also marked in the qPCR validation experiment with the insecticide-resistant lines exhibiting a higher proportion of bacteria from the phylum of Firmicutes and a lower proportion of Proteobacteria than the SS strain (Figure S4).

Bottom Line: Both insecticide-resistant lines had more Lactobacillales and the much scarcer taxa Pseudomonadales and Xanthomonadales with fewer Enterobacteriales compared with the susceptible strain.While this is consistent with the hypothesis that Lactobacillales or other scarcer taxa play a role in conferring DBM insecticide resistance, further studies are necessary to rule out other possibilities.Findings constitute the basis for future molecular work on the functions of insect midgut microbiota taxa and their possible role in conferring host resistance to toxins.

View Article: PubMed Central - PubMed

Affiliation: Institute of Applied Ecology, Fujian Agriculture and Forestry University, Fuzhou, China.

ABSTRACT

Background: Insect midgut microbiota is important in host nutrition, development and immune response. Recent studies indicate possible links between insect gut microbiota and resistance to biological and chemical toxins. Studies of this phenomenon and symbionts in general have been hampered by difficulties in culture-based approach. In the present study, DNA sequencing was used to examine the midgut microbiota of diamondback moth (DBM), Plutella xylostella (L.), a destructive pest that attacks cruciferous crops worldwide. Its ability to develop resistance to many types of synthetic insecticide and even Bacillus thuringiensis toxins makes it an important species to study.

Methodology/principal findings: Bacteria of the DBM larval midgut in a susceptible and two insecticide (chlorpyrifos and fipronil) resistant lines were examined by Illumina sequencing sampled from an insect generation that was not exposed to insecticide. This revealed that more than 97% of the bacteria were from three orders: Enterobacteriales, Vibrionales and Lactobacillales. Both insecticide-resistant lines had more Lactobacillales and the much scarcer taxa Pseudomonadales and Xanthomonadales with fewer Enterobacteriales compared with the susceptible strain. Consistent with this, a second study observed an increase in the proportion of Lactobacillales in the midgut of DBM individuals from a generation treated with insecticides.

Conclusions/significance: This is the first report of high-throughput DNA sequencing of the entire microbiota of DBM. It reveals differences related to inter- and intra-generational exposure to insecticides. Differences in the midgut microbiota among susceptible and insecticide-resistant lines are independent of insecticide exposure in the sampled generations. While this is consistent with the hypothesis that Lactobacillales or other scarcer taxa play a role in conferring DBM insecticide resistance, further studies are necessary to rule out other possibilities. Findings constitute the basis for future molecular work on the functions of insect midgut microbiota taxa and their possible role in conferring host resistance to toxins.

Show MeSH
Related in: MedlinePlus