The Evolution of Bacterial Mutualism with Eukaryotic Hosts

Bacteria: friend or foe?

All plants and animals share some form of intimate relationship with bacteria. Although we often focus on harmful bacteria that cause diseases, recent research has shown that many bacteria that live within animals are actually beneficial. Whether this is the light-producing bacteria that live within fireflies that help them attract mates to the 100 trillion bacterial cells that live within our guts that aid in digestion, beneficial microbes are both ever-present and important to all organisms on the planet.

My research explores how animals form beneficial relationships with symbiotic microbes by asking: What are the factors that produce stable mutually beneficial unions between animals and microbes, and what cause these relationships to break down? To answer these questions I focus on a single group of organisms that have evolved fascinating relationships with microbes, insects. Insects are host to a diverse community of symbiotic microbes that have profound effects on their biology. These effects include, protecting insects from natural enemies, such as parasitic wasp and pathogenic fungus, providing insects with protection against heat stress and assist insects in gaining nutrients.

A peculiar feature of these helpful microbes is that only certain populations of insects have them, whereas others do not. In addition, only certain bacterial strains provide benefits to their insect hosts whereas others do not. This natural variation presents a perfect opportunity to ask questions such as: why do certain populations of insect hosts contain beneficial microbes whereas others do not? And, why do only some of the symbiotic microbes provide benefits to insects, and how does the loss of beneficial function impact their relationship with their host?

To answer these questions I use modern DNA technology that allow me to identity factors that influence beneficial microbial functions at a molecular level, as well as explore the evolution of host-microbe relationships over millions of years. The application of these modern techniques to the intriguing variation in the bacterial symbionts of insects provides a general understanding of the factors that maintain and degrade beneficial relationships with bacteria in all plants and animals.

Host-microbe relationships are everywhere in nature, and understanding the factors that maintain and degrade these relationships has important implications in both agriculture and health. My research will not only provide novel insight into the gain and loss of beneficial traits in bacteria, but also has great potential in understanding the gain and loss of harmful traits in bacterial pathogens. Of more immediate application, my research can lead to practical solutions for managing insect pests in agriculture and those that vector major human diseases. Pesticides were common solutions to deal with pests, however there is strong pressure to reduce pesticide use to moderate our reliance on environmental harmful chemicals. Many insect pests have evolved mutualistic relationships with symbiotic bacteria such as, Triatoma bugs that vector Chagas disease, tsetse fly that vector sleeping sickness, cereal weevils that devastates crops around the world, and all sap sucking insects. Research to exploit the relationship between bacteria and insect hosts for the biological control of pests, termed Symbiont-Based Control Strategies, is a preferred strategy to chemical control due to the reduced environmental impact. My research is a critical first step in advancing our understanding of insect-bacteria relationships in many pest species, by revealing both the molecular mechanisms by which bacteria and hosts interact, as well as the conditions that promote stable relationships between bacteria and host. The knowledge from this research can be used to help develop practical solutions for managing pests in agriculture, forestry and those that vector major human diseases.

The proposed research is academic in nature and the primary beneficiaries will be the scientific community. However, aphids are one of the most damaging pests in agriculture in the European Union, and this research can translate to economic benefits if used by applied scientists to improve pest management. As such, potential beneficiaries include: 1) the pest control sector stands to benefit through the control of pests in agriculture, forestry and those that vector diseases in humans, and 2) the general public, through the use of this research as a tool to teach non-specialist audiences about insect biology and symbiosis.

Pest Control

Who will benefit? This research stands to benefit biocontrol companies, medical entomologists and practitioners that work in forestry and agriculture.

ow will they benefit? Pesticides are the chief method by which farmers deal with aphids, however there is strong pressure to reduce the use of environmentally damaging chemical pesticides. Knowledge from this research has potential to aid in managing pest through manipulating the relationship between symbiont and insect host. Many insect pests have evolved mutualistic relationships with symbiotic bacteria such as, Triatoma bugs that vector Chagas disease, tsetse fly that vector sleeping sickness and the cereal weevil that devastates cereal crops. Research to exploit symbiosis for the biological control of insect pests, termed Symbiont-Based Control Strategies (SCS), has great potential to move us away from chemical control. Over 150 SCS projects have been funded at a national level in Europe (COST Action 850). My research specifically addresses the EU mandate on applied SCS research by identifying both fitness gains in symbiotic partnerships (through bacterial mutualism) and the characterization of new molecular mechanisms. The results of this research directly contributes to the COST Action 850 initiative, which can be used to direct applied science in the management of pests in agriculture and those that vector important human diseases.

The public

Who will benefit? Gardeners, horticulturalists, farmers and the general public.

How will they benefit? During the fellowship I will use a number of outreach activities to engage the general public with my research as well as promote my findings to media. Results from the proposed research will be distributed through the Oxford Martin School Programme on the Future of Food. This initiative, directed by collaborator Prof Godfray, aims to link research at Oxford University on the food system, including, of relevance here, pest management.
Public outreach. In addition, I will work with Alison Foster (Senior Curator at the Botanic Garden) in developing lectures to be presented to the general public, which will include results from this research. Lectures will target non-specialist audience and teach insect biology, diversity and the importance of beneficial bacteria in the lives of insect and all animals and plants.
Media. Apart from the above outreach activities I will design a new webpage to present this research to a wide audience. I will also collaborate with Oxford University Press office to write press releases for all of my publications and be available for interviews and questions from journalists.