Nicotinoid and fungal disease team up to break down termites' tough defenses

May 20, 2015  


WEST LAFAYETTE, Ind. - Purdue University research shows that a small amount of nicotinoid pesticide substantially weakens termites' ability to fight off fungal diseases, a finding that could lead to more effective methods of pest control.

The study also provides clues into termites' robust defense systems and how nicotinoids affect social insects.

A team led by Michael Scharf, the O.W. Rollins/Orkin Chair and professor of entomology, found that a sublethal dose of imidacloprid knocked out key microbes in the termite gut and suppressed the social hygiene habits that help keep a termite colony healthy. Their defenses weakened, the termites became vulnerable to a fungal pathogen that normally poses little threat. The combination of pesticide and pathogen wiped out laboratory colonies in seven days.

"A termite colony can tolerate this dose of imidacloprid and fungal pathogen independently, but put them together, and they really have deleterious effects," Scharf said. "Understanding how to cripple termite defenses could lead us to new, safer control technologies."

Termites rarely get sick, despite living in moist, underground environments and in close contact with thousands of fellow colony members - conditions that are ideal for disease development.

While termites contain the disease defense genes common among all insects, they also have unique, non-genetic ways of protecting themselves from pathogenic bacteria and fungi, Scharf said.

Termites build up "social immunity" by grooming pathogens off of one another and transfer disease resistance throughout the colony by feeding on each other's secretions, said study co-author Drion Boucias, a professor of insect pathology at the University of Florida who has been researching termite immunity and response to disease for several decades.

"Social cleaning and grooming are critical," he said. "A solitary termite is susceptible to anything."

Termites also protect themselves by cultivating mutually beneficial relationships with microorganisms. The termite gut houses what Boucias called a "microbial garden" - a rich community of thousands of beneficial bacteria and protists, simple microorganisms whose symbiotic relationship coevolved with termites over millions of years. These microbes allow termites to digest cellulose, the tough material that gives plants their ability to stand upright. But they also appear to play an important role in disease defense.

Previous research suggests that some of these protists produce an enzyme that fatally punctures the cell wall of pathogenic invaders.

When Scharf and Boucias's team treated termite colonies with a small dose of imidacloprid, the protists began to die. The pesticide also had a druglike effect on termites, suppressing the grooming behaviors necessary to keep colony members from being infected with a fungal disease. 

Applying a sublethal amount of a fungal pathogen quickly destroyed the imidacloprid-treated colonies. The pathogen penetrated the termites' outer cuticle and dissolved their muscles and organs.

"The termites became little fuzzy piles of mush," Scharf said. "We don't typically see this in colonies in the wild unless they are severely stressed."

The researchers studied the termites' gut metatranscriptome - all termite and microbe genes that are being expressed at a given moment - to measure the decline of the gut microbes and better understand which genes are involved in termite defense.

Unexpectedly, the pesticide and fungus did not trigger the "stereotypical" immunity genes that they do in other insect species such as bees, Scharf said. The finding could indicate that termites rely almost exclusively on their gut microbes and social immunity to protect their health.

Future control measures may target these defenses, opening the door for termites' natural enemies to finish the job, Boucias said.

The paper was published in PloS One and is available at http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0123391

Funding for the research was provided by the U.S. Department of Agriculture's National Institute for Food and Agriculture and the O.W. Rollins/Orkin Endowment at Purdue. 

Writer:  Natalie van Hoose, 765-496-2050, nvanhoos@purdue.edu 

Sources: Michael Scharf, 765-496-6710, mscharf@purdue.edu

Drion Boucias, 352-273-3959, pathos@ufl.edu


ABSTRACT

Molecular signatures of nicotinoid-pathogen synergy in the termite gut

Ruchira Sen 1; Rhitoban Raychoudhury 1; Y. Cai 2; Yijun Sun 2; Verena Ulrike Lietze 3; Brittany F. Peterson 1; Michael E. Scharf 1; Drion G. Boucias 3

1 Department of Entomology, Purdue University, West Lafayette, IN, USA

2 Interdisciplinary Center for Biotechnology Research, University of Florida, Gainesville, FL, USA

3 Entomology and Nematology Department, University of Florida, Gainesville, FL, USA

E-mail: mscharf@purdue.edu 

Previous studies in lower termites revealed unexpected synergies between nicotinoid insecticides and fungal entomopathogens. The present study investigated molecular mechanisms of nicotinoid-pathogen synergy in the lower termite Reticulitermes flavipes, using the nicotinoid imidacloprid in combination with fungal and bacterial entomopathogens. Particular focus was placed on metatranscriptome composition and microbial dynamics in the symbiont-rich termite gut, which houses diverse mixes of protists and bacteria. cDNA microarrays containing a mix of host and protest symbiont oligonucleotides were used to simultaneously assess termite and protest gene expression. Five treatments were compared that included single challenges with sublethal doses of fungi (Metharizium anisopliae), bacteria (Serratia marcescens) or imidacloprid, and dual challenges with fungi + imidacloprid or bacteria + imidacloprid. Our findings point toward protest dysbiosis and compromised social behavior, rather than suppression of stereotypical immune defense mechanisms, as the dominant factors underlying nicotinoid-pathogen synergy in termites. Also, greater impacts observed for the fungal pathogen than for the bacterial pathogen suggest that the rich bacterial symbiont community in the R. flavipes gut (>5000 species-level phylotypes) exists in an ecological balance that effectively excludes exogenous bacterial pathogens. These findings significantly advance our understanding of antimicrobial defenses in this important eusocial insect group, as well as provide novel insights into how nicotinoids can exert deleterious effects on social insect colonies.  


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