Gut Microbiota Mediate Insecticide Resistance in the Diamondback Moth, Plutella xylostella (L.)

doi:10.3389/fmicb.2018.00025

. 2018 Jan 23:9:25.

doi: 10.3389/fmicb.2018.00025. eCollection 2018.

Gut Microbiota Mediate Insecticide Resistance in the Diamondback Moth, Plutella xylostella (L.)

Xiaofeng Xia^{1

2

3

4}, Botong Sun^{1

2

3

4}, Geoff M Gurr^{1

2

4

5}, Liette Vasseur^{1

2

4

6}, Minqian Xue^{1

2

3

4}, Minsheng You^{1

2

3

4}

Affiliations

¹ State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Institute of Applied Ecology, Fujian Agriculture and Forestry University, Fuzhou, China.
² Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, China.
³ Key Laboratory of Green Pest Control (Fujian Agriculture and Forestry University), Fujian Province University, Fuzhou, China.
⁴ Fujian-Taiwan Joint Centre for Ecological Control of Crop Pests, Fujian Agriculture and Forestry University, Fuzhou, China.
⁵ Graham Centre, Charles Sturt University, Orange, NSW, Australia.
⁶ Department of Biological Sciences, Brock University, Ontario, ON, Canada.

PMID: 29410659
PMCID: PMC5787075
DOI: 10.3389/fmicb.2018.00025

Gut Microbiota Mediate Insecticide Resistance in the Diamondback Moth, Plutella xylostella (L.)

Xiaofeng Xia et al. Front Microbiol. 2018.

. 2018 Jan 23:9:25.

doi: 10.3389/fmicb.2018.00025. eCollection 2018.

Authors

Xiaofeng Xia^{1

2

3

4}, Botong Sun^{1

2

3

4}, Geoff M Gurr^{1

2

4

5}, Liette Vasseur^{1

2

4

6}, Minqian Xue^{1

2

3

4}, Minsheng You^{1

2

3

4}

Affiliations

¹ State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Institute of Applied Ecology, Fujian Agriculture and Forestry University, Fuzhou, China.
² Joint International Research Laboratory of Ecological Pest Control, Ministry of Education, Fuzhou, China.
³ Key Laboratory of Green Pest Control (Fujian Agriculture and Forestry University), Fujian Province University, Fuzhou, China.
⁴ Fujian-Taiwan Joint Centre for Ecological Control of Crop Pests, Fujian Agriculture and Forestry University, Fuzhou, China.
⁵ Graham Centre, Charles Sturt University, Orange, NSW, Australia.
⁶ Department of Biological Sciences, Brock University, Ontario, ON, Canada.

PMID: 29410659
PMCID: PMC5787075
DOI: 10.3389/fmicb.2018.00025

Abstract

The development of insecticide resistance in insect pests is a worldwide concern and elucidating the underlying mechanisms is critical for effective crop protection. Recent studies have indicated potential links between insect gut microbiota and insecticide resistance and these may apply to the diamondback moth, Plutella xylostella (L.), a globally and economically important pest of cruciferous crops. We isolated Enterococcus sp. (Firmicutes), Enterobacter sp. (Proteobacteria), and Serratia sp. (Proteobacteria) from the guts of P. xylostella and analyzed the effects on, and underlying mechanisms of insecticide resistance. Enterococcus sp. enhanced resistance to the widely used insecticide, chlorpyrifos, in P. xylostella, while in contrast, Serratia sp. decreased resistance and Enterobacter sp. and all strains of heat-killed bacteria had no effect. Importantly, the direct degradation of chlorpyrifos in vitro was consistent among the three strains of bacteria. We found that Enterococcus sp., vitamin C, and acetylsalicylic acid enhanced insecticide resistance in P. xylostella and had similar effects on expression of P. xylostella antimicrobial peptides. Expression of cecropin was down-regulated by the two compounds, while gloverin was up-regulated. Bacteria that were not associated with insecticide resistance induced contrasting gene expression profiles to Enterococcus sp. and the compounds. Our studies confirmed that gut bacteria play an important role in P. xylostella insecticide resistance, but the main mechanism is not direct detoxification of insecticides by gut bacteria. We also suggest that the influence of gut bacteria on insecticide resistance may depend on effects on the immune system. Our work advances understanding of the evolution of insecticide resistance in this key pest and highlights directions for research into insecticide resistance in other insect pest species.

Keywords: diamondback moth; gut bacteria; immunity; microbial symbionts; pleiotropic effects.

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Figures

**Figure 1**
Changes in relative abundance of *P. xylostella* gut bacteria after consuming cabbage leaves inoculated with Enterobacteriaceae, *Serratia*, and *Enterococcus*. CK, control; error bars are standard deviation (SD), ^** indicates significant difference at P < 0.01.

**Figure 2**
Effect of gut bacteria and compounds on mediation of insecticide resistance in *P. xylostella*. **(A)** Effects of live gut bacteria in mediation of resistance to chlorpyrifos; **(B)** effect of heat-killed gut bacteria in mediation of resistance to chlorpyrifos; and **(C)** effects of vitamin C and acetylsalicylic acid on mediation of resistance to chlorpyrifos. Eb, *Enterobacter* sp.; Sm, *Serratia* sp.; Ec, *Enterococcus* sp.; Ab, antibiotics; Vc, vitamin C, Ap, acetylsalicylic acid; and CK, control. Error bars are SD.

**Figure 3**
Degradation efficiency of *P. xylostella* gut bacteria on chlorpyrifos. **(A)** Standard curve of chlorpyrifos detected by ultraviolet spectrophotometry under OD₂₉₃ nm; **(B)** degradation efficiency of chlorpyrifos by different gut bacteria. Eb, *Enterobacter* sp.; Sm, *Serratia* sp.; Ec, *Enterococcus* sp.; and CK, control. Error bars are SD; n.s. indicates no significant difference.

**Figure 4**
Effect of live gut bacteria on expression of AMPs in *P. xylostella*. **(A)** Expression of lysozyme; **(B)**, expression of moricin; **(C)** expression of gloverin; and **(D)** expression of cecropin. Eb, *Enterobacter* sp.; Sm, *Serratia* sp.; Ec, *Enterococcus* sp.; Ab, antibiotics; and CK, control. Error bars are SD.

**Figure 5**
Effect of heat-killed gut bacteria on expression of AMPs in *P. xylostella*. **(A)** Expression of lysozyme; **(B)** expression of moricin; **(C)** expression of gloverin; and **(D)**: expression of cecropin. Eb, heat-killed *Enterobacter* sp.; Sm, heat-killed *Serratia* sp.; Ec, heat-killed *Enterococcus* sp.; and CK, control. Error bars are SD.

**Figure 6**
Effect of compounds on expression of AMPs in *P. xylostella*. **(A)** Expression of lysozyme; **(B)** expression of moricin; **(C)** expression of gloverin; and **(D)** expression of cecropin. Vc, vitamin C, Ap: acetylsalicylic acid; and CK, control. Error bars are SD.

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References

1. Broderick N. A., Raffa K. F., Handelsman J. (2006). Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc. Natl. Acad. Sci. U.S.A. 103, 15196–15199. 10.1073/pnas.0604865103 - DOI - PMC - PubMed
1. Broderick N. A., Raffa K. F., Handelsman J. (2010). Chemical modulators of the innate immune response alter gypsy moth larval susceptibility to Bacillus thuringiensis. BMC Microbiol. 10:129. 10.1186/1471-2180-10-129 - DOI - PMC - PubMed
1. Broderick N. A., Raffa K. F., Goodman R. M., Handelsman J. (2004). Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl. Environ. Microb. 70, 293–300. 10.1128/AEM.70.1.293-300.2004 - DOI - PMC - PubMed
1. Broderick N., Goodman R., Handelsman J., Raffa K. (2003). Effect of host diet and insect source on synergy of gypsy moth (Lepidoptera: Lymantriidae) mortality to Bacillus thuringiensis subsp. kurstaki by zwittermicin A. Environ. Entomol. 32, 387–391. 10.1603/0046-225X-32.2.387 - DOI
1. Broderick N., Robinson C., McMahon M., Holt J., Handelsman J., Raffa K. (2009). Contributions of gut bacteria to Bacillus thuringiensis-induced mortality vary across a range of Lepidoptera. BMC Biol. 7:11. 10.1186/1741-7007-7-11 - DOI - PMC - PubMed

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[1] Broderick N. A., Raffa K. F., Handelsman J. (2006). Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc. Natl. Acad. Sci. U.S.A. 103, 15196–15199. 10.1073/pnas.0604865103 - DOI - PMC - PubMed

[2] Broderick N. A., Raffa K. F., Handelsman J. (2006). Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc. Natl. Acad. Sci. U.S.A. 103, 15196–15199. 10.1073/pnas.0604865103 - DOI - PMC - PubMed

[3] Broderick N. A., Raffa K. F., Handelsman J. (2010). Chemical modulators of the innate immune response alter gypsy moth larval susceptibility to Bacillus thuringiensis. BMC Microbiol. 10:129. 10.1186/1471-2180-10-129 - DOI - PMC - PubMed

[4] Broderick N. A., Raffa K. F., Handelsman J. (2010). Chemical modulators of the innate immune response alter gypsy moth larval susceptibility to Bacillus thuringiensis. BMC Microbiol. 10:129. 10.1186/1471-2180-10-129 - DOI - PMC - PubMed

[5] Broderick N. A., Raffa K. F., Goodman R. M., Handelsman J. (2004). Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl. Environ. Microb. 70, 293–300. 10.1128/AEM.70.1.293-300.2004 - DOI - PMC - PubMed

[6] Broderick N. A., Raffa K. F., Goodman R. M., Handelsman J. (2004). Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl. Environ. Microb. 70, 293–300. 10.1128/AEM.70.1.293-300.2004 - DOI - PMC - PubMed

[7] Broderick N., Goodman R., Handelsman J., Raffa K. (2003). Effect of host diet and insect source on synergy of gypsy moth (Lepidoptera: Lymantriidae) mortality to Bacillus thuringiensis subsp. kurstaki by zwittermicin A. Environ. Entomol. 32, 387–391. 10.1603/0046-225X-32.2.387 - DOI

[8] Broderick N., Goodman R., Handelsman J., Raffa K. (2003). Effect of host diet and insect source on synergy of gypsy moth (Lepidoptera: Lymantriidae) mortality to Bacillus thuringiensis subsp. kurstaki by zwittermicin A. Environ. Entomol. 32, 387–391. 10.1603/0046-225X-32.2.387 - DOI

[9] Broderick N., Robinson C., McMahon M., Holt J., Handelsman J., Raffa K. (2009). Contributions of gut bacteria to Bacillus thuringiensis-induced mortality vary across a range of Lepidoptera. BMC Biol. 7:11. 10.1186/1741-7007-7-11 - DOI - PMC - PubMed

[10] Broderick N., Robinson C., McMahon M., Holt J., Handelsman J., Raffa K. (2009). Contributions of gut bacteria to Bacillus thuringiensis-induced mortality vary across a range of Lepidoptera. BMC Biol. 7:11. 10.1186/1741-7007-7-11 - DOI - PMC - PubMed

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Gut Microbiota Mediate Insecticide Resistance in the Diamondback Moth, Plutella xylostella (L.)

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Gut Microbiota Mediate Insecticide Resistance in the Diamondback Moth, Plutella xylostella (L.)

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