How an Entomologist Explores the Bacterial Saboteurs of Insect Reproduction
By Lorena Lopez, Ph.D.
Editor’s Note: This is the next post in the “Standout ECPs” series contributed by the Entomological Society of America’s Early Career Professionals (ECP) Committee, highlighting outstanding ECPs that are doing great work in the profession. (An ECP is defined as anyone within the first five years of obtaining their terminal degree in their field.) It is also the third in a set of four featuring ECPs selected to present their work during the ECP Recognition Symposium at the 2022 Joint Annual Meeting of the Entomological Societies of America, Canada, and British Columbia, November 13-16, in Vancouver. Read past posts in the Standout ECPs series.
Matt Doremus, Ph.D., was recently hired as a postdoctoral researcher at the University of Kentucky, where he works with an emerging spider model system for studying heritable symbiont communities. Previously, Doremus spent one year as a postdoctoral associate at the University of Arizona where he worked on identifying symbiont genetic factors involved in a manipulative symbiosis. He earned his bachelor’s degree in biology and entomology from the University of Georgia in 2014, his master’s in entomology from the same institution in 2016, and his Ph.D. in entomology from the University of Arizona in 2021, where he studied how the common maternally transmitted bacterial symbiont Cardinium manipulates its parasitoid wasp host’s reproduction and how the external environment affects this symbiosis.
Doremus was selected to present his research at the ECP Recognition Symposium at the 2022 Joint Annual Meeting of the Entomological Societies of America, Canada, and British Columbia, November 13-16, in Vancouver. His presentation in the symposium, titled “Cardinium-induced cytoplasmic incompatibility in Encarsia parasitoid wasps,” is slated for 10:50 a.m. Pacific Time, on Tuesday, November 15.
Lopez: Can you describe your current research?
Doremus: I study arthropod-microbe symbioses, and my work has focused on the ecology and evolution of heritable, maternally transmitted symbionts. These symbionts, usually intracellular bacteria, infect most arthropods and can have fundamental impacts on arthropod biology, whether by fulfilling nutritional roles for diet-limited hosts, providing resistance to natural enemies, or manipulating host reproduction to favor infected females.
Since these bacteria are usually transmitted by females, this sabotage often comes at the expense of male hosts or uninfected individuals. The most common form of manipulation is cytoplasmic incompatibility (CI), a form of reproductive sabotage in which the symbiont uses male hosts to kill the offspring of uninfected females. This sabotage is a two-step process: First, it somehow modifies infected males to deliver a lethal factor into eggs during mating, killing the offspring. Next, when the male mates with an infected female, the symbiont reverses this lethal modification in the egg and rescues the offspring, which survive. This phenomenon gives infected females a reproductive advantage at the cost of uninfected females, and so the symbiont spreads rapidly in a population.
Their ability to drive themselves and desirable traits (like pathogen resistance) to high frequencies has made CI-inducing symbionts a promising avenue for pest population control. Most of this work has focused on the widespread symbiont Wolbachia, which, in addition to causing CI, also increases mosquito resistance to human pathogens like the Dengue virus. However, beyond Wolbachia, our understanding of symbiont-induced CI is limited.
While heritable symbioses are common, the symbionts themselves usually have a limited ability to respond to stress and are thermally sensitive. Temperature stress often causes a reduction of symbiont numbers in their host, the failure of symbiont-conferred phenotypes, and a reduction in symbiont transmission rate. These effects can slow the spread of symbionts or cause once-stable symbioses to be lost. My research focuses on how manipulative symbionts sabotage arthropod reproduction and how temperature affects the stability of these symbioses.
For my dissertation research, I worked with Dr. Molly Hunter at the University of Arizona on CI caused by the common symbiont Cardinium hertigii, which infects approximately 7–10 percent of arthropod species. I studied how temperature stress affects Cardinium CI and the stability of Cardinium symbioses in Encarsia parasitoids, which are minute (less than 1 millimeter long) chalcidid parasitoid wasps of whiteflies. I found that exposure to temperature stress, specifically during the wasp pupal stage, affected the severity of CI, suggesting that the pupal stage was important for CI induction. Using fluorescent imaging on dissected testes (male wasps’ sperm-producing organs), I next found that Encarsia wasps produce most of their lifetime sperm during their pupal stage. Additionally, while Cardinium infects developing sperm, the symbiont is removed from the cell along with most of the cellular contents in the final stages of sperm development in Encarsia suzannae. However, in another Encarsia species, E. partenopea, Cardinium doesn’t infect sperm at all; instead, it infects the seminal vesicle, which is the storage organ that houses mature sperm.
Together, these results suggested that Cardinium specifically sabotages the sperm of male hosts during the pupal stage, although Cardinium strains may use different methods to perform this modification in different wasp species. We’re now using this information on the timing of CI induction to identify the Cardinium proteins responsible for CI and their host targets. This dissertation work has been published in several journals including Heredity, PLOS Pathogens, and Frontiers in Microbiology.
I’m now a postdoctoral researcher at the University of Kentucky, working on a new system that consists of the heritable symbiont community of the spider Mermessus fradeorum with Dr. Jen White. This spider species can host as many as five different heritable symbionts simultaneously, making it an excellent system to study how temperature can affect symbiont communities within hosts. Most spiders harbor a newly described CI symbiont, Rickettsiella, which is also a common symbiont of ticks. As this CI phenotype has only been described in the past couple of years, almost nothing is known about how Rickettsiella causes CI nor how the environment affects this symbiosis. In addition to Rickettsiella, these spiders can also harbor three strains of Wolbachia and a fifth symbiont called Tisiphia.
When spiders have all five symbionts, they are feminized so that genetic males develop as functional females capable of spreading these symbionts. We think this feminization requires Tisiphia, but Tisiphia alone cannot feminize spiders, suggesting that feminization requires the cooperation of multiple symbionts. I hope to explore how temperature alters the community dynamics of these symbionts and use comparative genomics to learn more about how these symbionts feminize their spider hosts, how Rickettsiella causes CI, and how these manipulative phenotypes evolved.
What’s your favorite aspect of your research?
I loved getting to use fluorescent microscopy to see Cardinium! Since the bacteria I study can’t be cultured normally, usually we use PCR to confirm infection. It’s one thing to see a band on a gel, it’s a whole other experience seeing the bacteria themselves inside host tissues! I also really enjoy working directly with the animals; both the wasps and the spiders have cool behaviors and biology. Watching parasitoid larvae slowly consume their host is crazy (and gruesome, I guess), and since whiteflies are translucent you can see almost the whole process.
What’s a recent research challenge you had to overcome, and how did you do it?
While we now understand a bit more about when Cardinium sabotages male hosts and what cells it targets, the proteins responsible for Cardinium CI continue to elude us. We’re taking a proteomics approach to identify these factors in Encarsia testes; the main problem is that Encarsia is a tiny wasp, and we needed enough tissue for reliable protein identification. I managed to figure out a way to dissect testes and successfully transport them to our collaborators (Manuel Kleiner’s lab at North Carolina State University), who will start working on the actual proteomics.
I dissected so, so many Encarsia this past year. I had to switch to decaf coffee; I couldn’t dissect them when I was caffeinated. You’d try to move the wasp and end up flicking it out a window. But it’ll be worth it if we can learn more about how Cardinium is manipulating these wasps!
If you could go back in time, what advice would you give to your graduate student self?
Take care of yourself and find a good work-life balance. Go home at 5 p.m.; nothing good happened to me in the lab after 5 p.m. anyway.
What is one thing you would change about the field of entomology?
It’s not really a change, but I think the continued commitment to fostering and maintaining diversity and inclusivity will be essential for entomology in the 21st century. We’re faced with impressive challenges to food production, human health, biodiversity, and climate adaptation over the next century, and having entomologists with diverse backgrounds and ideas will help us rise to these challenges.
What’s the coolest thing about your job that you wish more people knew?
I think the bugs themselves are cool, but the symbionts that manipulate them are crazy! I wish more people knew the extent the microbes dictate their host’s biology. Some of these bacteria can control whether a bug is male or female, or if their offspring will survive or not. Some can turn their hosts asexual! This is the stuff of science fiction and it’s real!
2022 Joint Annual Meeting of the Entomological Societies of America, Canada, and British Columbia, November 13-16, Vancouver
Lorena Lopez, Ph.D., is a postdoctoral researcher at Virginia Tech Department of Entomology’s Eastern Shore Agricultural Research and Extension Center and chair of the ESA Early Career Professionals Committee. Twitter: @lorelopez257. Email: email@example.com.
All photos courtesy of Matt Doremus, Ph.D., unless otherwise noted.