Every animal harbors a microbial community that can include pathogens and the commensal/beneficial microbiota; therefore, managing and maintaining relationships with microorganisms has critically shaped the evolution of animals. My research explores: What forces drive the assembly of microbial communities? and How do microbes alter their host? Working at the axes of organismal biology, ecology and microbiology I utilize aspects of each to identify patterns of microbe-host association in nature and experimentally manipulate those associations. This work incorporates 1) environmental DNA sampling methods (16S rRNA, metagenomics) to observe microorganisms in their native environment, 2) culturing microbes and genome sequencing to identify metabolic features and 3) experimental manipulation of the microbes and their hosts to discover the consequences of host-microbe associations.
My focus is the microbial associates of insects, the most diverse group of animals, which are incredibly important in terrestrial ecosystem ecology, in agricultural systems as pests and pollinators, and in human health as vectors for disease.
My focus is the microbial associates of insects, the most diverse group of animals, which are incredibly important in terrestrial ecosystem ecology, in agricultural systems as pests and pollinators, and in human health as vectors for disease.
Invertebrates, and specifically insects are the most taxonomically diverse group of animals with an estimated 2.5 million species. They also represent the deadliest group of animals by vectoring human diseases and the costliest group to society by annually destroying 10-16% of agricultural crops world-wide. And yet many insects are beneficial, providing $67 billion/yr in services to the US alone: bees provide unmatched pollination services for crops, decomposers recycle nitrogen, and parasitoids are vital biocontrol agents for pests. Understanding the microbiota in insects and manipulating it to promote and protect beneficial insects and to kill and control pests represents a critical area in microbiota research.
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Current Projects
Beetle-Fungus symbiosis
Restoring a ‘Forgotten’ model organism – The Drugstore beetle and the Cigarette beetle (Coleoptera: Anobiidae) have specialized cells (mycetocytes) in their digestive tract that are infected by symbiotic fungi (Symbiotaphrina), which provide B vitamins and sterols. Unlike most symbiotic associations, Symbiotaphrina are transmitted extracellularly between generations on the surface of eggs, but live intracellularly in larvae and adults. Beetle mycetocytes are infected by the symbiont anew each generation, but because both beetles and fungi can be grown in axenic culture, novel host-symbiont pairs can be experimentally established. Because of this unique feature, these beetle-fungus mutualisms were foundational in early symbiosis research; however, they have been largely ignored for over 40 years.
Honey bee microbiota variation
Microorganisms benefit honey bee (Apis mellifera) health by increasing body weight, altering immune signaling, and providing resistance to pathogens. The high genetic and metabolic diversity of bacterial strains found in the honey bee gut may benefit the host by providing more redundancy and/or novel capabilities, however, the use of antibiotics for treating disease in US honey bees may have greatly reduced or altered the taxonomic and functional diversity of the microbiota through strong selection for resistance. The resulting microbiome imbalance may be contributing to honey bee colony loss, but supplementation with beneficial microbes may be a viable treatment.
Apis mellifera alone has many geographically widespread subspecies (e.g. Middle East, Asia, European, African), and the genus Apis includes 8 species, all of which host genetically diverse microbiota symbionts that may provide benefits not found in the US honey bee pan-microbiome. |
Microbiota-invertebrate relationships & ecology
Invertebrates compose ~70% of the described eukaryotic species and are incredibly abundant in nearly every environment. Many invertebrates are also invasive pests, yet microbiota research has not reached the majority these organisms. The microbial diversity associated with invertebrates represents a reservoir of novel microbes that actively interact with animal hosts. Observing and testing these microbes could broaden our insight of endosymbiotic bacterial lineages (eg. Wolbachia, Spiroplasma) and lead to the discovery of natural pathogens that could be used as biocontrol agents.
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Previous Research
Symbiotic gut microbes of honey bees
Working with the newly sequenced honey bee genome and an international group of researchers, my advisor, Nancy Moran, and I discovered that A. mellifera universally harbor a symbiotic microbiota of 9 bacteria (Cox-Foster et al. 2007). These bacteria account for >96% of an individual’s microbiota and form a biofilm in the hindgut (Martinson et al. 2012). There is substantial strain variation within each of the 9 microbiota bacteria, suggesting that complex microbial competition and coordination occurs within the honeybee gut (Engel, Martinson, Moran 2012). Bumblebees share a characteristic microbiota with honeybees, but other bee species (solitary breeders) do not, suggesting that sociality is a factor in the evolution of a consistent microbiota (Martinson et al. 2011; Martinson et al. 2014).
Honey bees (Apis mellifera) are a major influence on agricultural ecosystem productivity as the central pollinator of many crops. US beekeepers have experienced abnormally high hive mortality since 2006, the cause of which is still unknown. As in other animals, the microbiota plays a large role in general health, yet the honeybee’s natural microbiome is understudied and many of their host-symbiont relationships are functional uncharacterized. I think that future research on the honeybee microbiota may provide insights into the cause of colony declines and discover potential treatment options. |
Microbial ecology in wild Drosophila
Unlike Drosophila melanogaster, most of the >1500 described Drosophila species have a specialized diet (e.g. mushrooms, cactus, tree sap) and are geographically restricted. Native species can be collected in nearly every ecosystem around the world and these flies can be reared in the lab. Working with John Jaenike at the University of Rochester I performed population microbiota surveys of native, wild-caught Drosophila species and their food substrates. Similar to vertebrates, there was high variation in microbiota composition between individuals, but using ecological models I found that individual flies did not have random communities. Instead, certain bacteria (including members of the Orbales) specifically colonized the insect gut but not their dietary resources (Figure). This was found in both mushroom- and cactus-feeding species in New York and Mexico, suggesting that it is a broad pattern in the wild Drosophila microbiota (Martinson et al. 2017ab). In an effort to find functional interactions between the host and microbiota, I helped analyze transcriptomes (fly) and metagenomes (microbiota) and found links between gut metabolism and the microbiota (Bost et al. 2018ab).
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Functional interactions in the mosquito-microbiota relationship
Ecological research on wild mosquito food chains dating back several decades found that larvae are important microbivores that reduce microbe populations in their natural habitats. Recently it was found that bacteria and other microbes residing in the mosquito larvae gut provide signals that are required for larval development (Coon et al. 2017, Valzania et al. 2018). Integrating mosquito ecology and natural history with the recent discovery that microbes are required for mosquito development, I performed gnotobiotic experiments to address the central question: How do interactions between microbial community composition and diet quality affect mosquito development?
More research to come from my work in Mike Strand’s lab at the University of Georgia. |