Wasps' gut microbes help them -- and their offspring -- survive pesticides

February 04, 2020

Exposure to the widely used pesticide atrazine leads to heritable changes in the gut microbiome of wasps, finds a study publishing February 4 in the journal Cell Host & Microbe. Additionally, the altered microbiome confers atrazine resistance, which is inherited across successive generations not exposed to the pesticide.

"After a single exposure to some chemicals--xenobiotics--the gut microbiome can be permanently affected," says senior study author Robert Brucker of Harvard University. "Exposure can have lasting changes to future generations even after an exposure risk is eliminated."

Agrochemicals used to fertilize crops and control pest species pose one of the greatest xenobiotic exposure risks to many organisms. The herbicide atrazine is the second most sold pesticide globally. Previous studies have shown that atrazine has multiple effects on host animals, but little is known about how environmental xenobiotic chemicals change the gut microbiome.

To address this question, Brucker and his team examined the impact of acute or continuous subtoxic atrazine exposure on the model wasp species Nasonia vitripennis across 36 generations. Analysis of the transcriptome and proteome of the wasps revealed that exposure to 300 parts per billion (ppb) of atrazine--similar to the concentration encountered by pollinators in newly sprayed agricultural fields and streams--may alter N. vitripennis immunity, mitochondrial function, and behavior.

In the first generation, exposure to 300 ppb of atrazine altered the bacterial community structure of wasps, resulting in an increase in microbiome diversity and overall bacterial load. Even exposure to a lower concentration of 30 ppb of atrazine caused a microbiome shift that persisted across successive generations.

When the researchers switched the offspring of the atrazine-exposed population to a non-atrazine diet for six generations, they observed that the bacterial microbiome remained most similar to that of the parents. "This result indicates that the disruption to the microbiome after acute exposure to atrazine is inherited across generations, even after exposure is removed," Brucker says.

In addition, exposure to 30 ppb of atrazine over 36 generations reduced atrazine-induced mortality by a factor of ten, and also increased tolerance to the herbicide glyphosate, despite no prior exposure to the compound. After 25 generations, a subset of the wasp population was switched to a non-atrazine diet. Remarkably, atrazine tolerance was inherited and sustained through the 36th generation.

Other experiments showed that the increased atrazine tolerance of wasps is related to their altered microbiome. For example, maintaining wasps in a germ-free environment eliminated atrazine tolerance. On the other hand, transplanting the microbiome of atrazine-exposed wasps to non-exposed wasps conferred atrazine resistance.

"Overall, we demonstrate that resistance to multiple pesticides can arise in a population that is exposed to sub-toxic concentrations, that the microbiome facilitates this resistance, and that it provides resistance against other pesticides to which the host animal has never been previously exposed," Brucker says.

In particular, atrazine exposure increased the densities of the rare gut bacteria Serratia marcescens and Pseudomonas protegens. Feeding these atrazine-degrading bacteria to wasps that had not been exposed to atrazine resulted in resistance to this pesticide.

"The shift in the microbial community following continuous atrazine exposure may be providing host resistance via detoxification, representing a rapid route of ecological adaptation for the host to cope with novel toxic challenges," Brucker says. "Pesticide exposure causes functional, inherited changes in the microbiome that should be considered when assessing xenobiotic exposure and as potential countermeasures to toxicity."

Taken together, the findings demonstrate that atrazine exposure can alter the microbial community of wasps, which can in turn directly impact host fitness across generations. Even though Nasonia wasps are not natural crop pollinators, the study could have broad implications. Wild populations of pollinators have been exposed to atrazine since the 1950s, the equivalent of dozens of generations. Notably, bacterial atrazine-metabolizing genes are also present in wild bee populations exposed to the pesticide.

"These results could reflect microbe-host-associated changes in response to xenobiotic exposure in wild honey bee population, similar to what we describe in Nasonia and considering the decades of habitual exposure, and adaptation within pollinator populations are likely to have already occurred," Brucker says. "Ultimately, these effects could have repercussions on host behavior, metabolic stress, immunocompetence, and host-microbiota regulation."

In future studies, Brucker and his team plan to examine which loci have been under selection, and how they might be implicated in toxin resistance or microbiome regulation. They are also planning on leveraging their findings to develop probiotics for honey bees to reduce multi-pesticide exposure risk.

"We can use our understanding of the host-microbiome interaction to reduce the exposure risk of all pesticides, for example, by using bacteria for cleaning up spills or as probiotics for at-risk humans, or off-target plants and animals," Brucker says. "Further host-microbiome studies of multi-generational exposure to xenobiotic compounds are needed, especially in light of the increased risk of xenobiotic exposure to humans, plants, animals, fungi, and bacteria across the globe."
This work was supported by a Rowland Institute at Harvard Fellowship.

Cell Host & Microbe, Wang et al.: "Changes in microbiome confer multigenerational host resistance after sub-toxic pesticide exposure" https://www.cell.com/cell-host-microbe/fulltext/S1931-3128(20)30048-2

Cell Host & Microbe (@cellhostmicrobe), published by Cell Press, is a monthly journal that publishes novel findings and translational studies related to microbes (which include bacteria, fungi, parasites, and viruses). The unifying theme is the integrated study of microbes in conjunction and communication with each other, their host, and the cellular environment they inhabit. Visit: http://www.cell.com/cell-host-microbe. To receive Cell Press media alerts, contact press@cell.com.

Cell Press

Related Science Articles from Brightsurf:

75 science societies urge the education department to base Title IX sexual harassment regulations on evidence and science
The American Educational Research Association (AERA) and the American Association for the Advancement of Science (AAAS) today led 75 scientific societies in submitting comments on the US Department of Education's proposed changes to Title IX regulations.

Science/Science Careers' survey ranks top biotech, biopharma, and pharma employers
The Science and Science Careers' 2018 annual Top Employers Survey polled employees in the biotechnology, biopharmaceutical, pharmaceutical, and related industries to determine the 20 best employers in these industries as well as their driving characteristics.

Science in the palm of your hand: How citizen science transforms passive learners
Citizen science projects can engage even children who previously were not interested in science.

Applied science may yield more translational research publications than basic science
While translational research can happen at any stage of the research process, a recent investigation of behavioral and social science research awards granted by the NIH between 2008 and 2014 revealed that applied science yielded a higher volume of translational research publications than basic science, according to a study published May 9, 2018 in the open-access journal PLOS ONE by Xueying Han from the Science and Technology Policy Institute, USA, and colleagues.

Prominent academics, including Salk's Thomas Albright, call for more science in forensic science
Six scientists who recently served on the National Commission on Forensic Science are calling on the scientific community at large to advocate for increased research and financial support of forensic science as well as the introduction of empirical testing requirements to ensure the validity of outcomes.

World Science Forum 2017 Jordan issues Science for Peace Declaration
On behalf of the coordinating organizations responsible for delivering the World Science Forum Jordan, the concluding Science for Peace Declaration issued at the Dead Sea represents a global call for action to science and society to build a future that promises greater equality, security and opportunity for all, and in which science plays an increasingly prominent role as an enabler of fair and sustainable development.

PETA science group promotes animal-free science at society of toxicology conference
The PETA International Science Consortium Ltd. is presenting two posters on animal-free methods for testing inhalation toxicity at the 56th annual Society of Toxicology (SOT) meeting March 12 to 16, 2017, in Baltimore, Maryland.

Citizen Science in the Digital Age: Rhetoric, Science and Public Engagement
James Wynn's timely investigation highlights scientific studies grounded in publicly gathered data and probes the rhetoric these studies employ.

Science/Science Careers' survey ranks top biotech, pharma, and biopharma employers
The Science and Science Careers' 2016 annual Top Employers Survey polled employees in the biotechnology, biopharmaceutical, pharmaceutical, and related industries to determine the 20 best employers in these industries as well as their driving characteristics.

Three natural science professors win TJ Park Science Fellowship
Professor Jung-Min Kee (Department of Chemistry, UNIST), Professor Kyudong Choi (Department of Mathematical Sciences, UNIST), and Professor Kwanpyo Kim (Department of Physics, UNIST) are the recipients of the Cheong-Am (TJ Park) Science Fellowship of the year 2016.

Read More: Science News and Science Current Events
Brightsurf.com is a participant in the Amazon Services LLC Associates Program, an affiliate advertising program designed to provide a means for sites to earn advertising fees by advertising and linking to Amazon.com.