| About MBL Astrobio | ||||
|---|---|---|---|---|
|
|
Other sites |
||||
|---|---|---|---|---|
|
Without the establishment of ancient bacterial endosymbioses, life as we know it today would be unrecognizable. From the origin of the eukaryotic cell to the formation of entirely new ecosystems, ancient endosymbioses initiated several major evolutionary and ecological transitions in the history of Life. Today, young systems of endosymbiotic bacteria are still formidable players in shaping Life, spurring on the evolution of incipient organelles and posing threats to the reproductive strategies of their animal hosts. It has been hypothesized that these younger associations may even act as a source of microevolutionary innovation for their hosts, leading to differentiation between host populations and ultimately to the evolution of new species. Using a natural system, comparative genomics, molecular evolution, and classical genetics, I study how endosymbiosis and speciation operate as separate and connected processes in evolution. I am particularly interested in drawing general conclusions about the early genomic events that shape endosymbiotic lifestyle, the role of endosymbiosis in the origin of new species, and the evolution of symbiont-host genome interactions.
How do the genomes of parasites and mutualists evolve in endosymbionts?
Investigating the genomic basis of young endosymbiotic associations (mutualism, commensalism, parasitism) can help elucidate how genomic events such as lateral transfer, gene loss, and recombination shape the evolution of parasitism and mutualism in endosymbionts. One such young endosymbiotic system is Wolbachia — a genus of alpha-Proteobacteria that groups phylogenetically with the bacterial ancestor of mitochondria and is the dominant endosymbiotic bacteria on the planet, occurring in up to 75% of all insect species, as well as other arthropods and filariid nematodes. They are influential passengers in their animal hosts, and potentially affect key evolutionary processes such as sex determination, sexual selection, and speciation. Unlike many endosymbiotic bacteria that are long-term mutualists within a limited host range, Wolbachia notably show more labile interactions that span the spectrum of intracellular lifestyles — from strict mutualism in filariid nematodes to reproductive parasitism in arthropods. Recent studies show that the Wolbachianaturally residing in filariid nematode cells are also causative agents of River Blindness in humans and enter the human blood system. I am particularly interested in using the natural plasticity in Wolbachia lifestyle to distinguish the incipient genomic events that shape endosymbionts into harmful parasites or long-term mutualists. I address this challenge through multifarious genetic methods and key collaborations with scientists from the Marine Biological Lab, The Institute for Genomic Research, University of Milan, University of Edinburgh, Boston University, and University of Rochester. Below are three projects that I am actively working on as part of a long-term research program on endosymbiont genome evolution.
Molecular phylogenies of Wolbachia showing their relationship to other intracellular alpha-Proteobacteria and the various taxonomic lineages (A-F) that comprise the Wolbachia genus. In the latter, host species names are used.
Project 1 uses phylogenetic and molecular evolution techniques to determine the direction of evolution of intracellular parasitism and mutualism, i.e., which arose first during the diversification of this thriving endosymbiosis. With a comprehensive sequencing approach and rigorous phylogenetic and statistical methods, we are retracing the evolution of parasitism and mutualism in these intracellular associations. Findings from this project will also decipher the original host for the ancestor of Wolbachia and the direction of bacterial transfer between the two host phyla (Nematoda and Arthropoda). Project 2 examines the evolution of an active bacteriophage that infects the Wolbachia parasitic genomes. In contrast to the genomes of mutualistic endosymbionts that traditionally show strict vertical transmission and efficient streamlining of selfish and mobile DNA, we predict that the genomes of more labile endosymbionts, that for instance undergo some horizontal transmission, may show more chromosomal plasticity. Recent progress from genomic studies of the parasitic Wolbachia that host-switch indicate bacteriophages are surprisingly common, laterally transfer between distantly related genomes, and recombine at high rates. Findings of horizontal transfer in endosymbiont communities are unexpected and raise innovative questions about whether phages are important contributors to endosymbiont diversification. Project 3 uses comparative genomic techniques to profile genome size and gene content variability in order to qualify the extent of gene acquisition and loss during an endosymbiont radiation. Specific events of genome flux will be mapped onto the bacterial phylogeny to determine when these events occurred and how large they were. Findings will also have implications for understanding the early events that shape some endosymbionts into new organelles and others into harmful passengers.
How important are genome interactions between endosymbionts and hosts?
Genome interactions are expected from coevolution, host responses to bacterial-imposed loads, and cytonuclear conflict. These interactions may manifest themselves as gene loss events, host suppression of bacterial phenotypes, endosymbiont-host codependence, and gene transfer from endosymbiont to host. The latter may be especially common and profoundly important to host genome evolution, since endosymbionts are often intimately associated with host cells in the germline. Our work shows that Wolbachia can be a significant source of evolutionary pressure in insect hosts. Parasitism poses a severe fitness cost to hosts and can be strongly affected by host genes. These findings coupled with other studies indicate that prokaryotic-eukaryotic genome interactions are common to invertebrate endosymbioses and have the potential to accelerate evolutionary change. Future goals of my research program will be to (i) identify the extent of candidate genes transferred from endosymbionts to the host nucleus using microarrays (ii) dissect the number and location of host chromosomal regions that interact with endosymbionts and (iii) profile expression variability of endosymbiont genes that interact with the host cytoplasmic environment, with particular interest in associations between gene expression and lifestyle variation.Does endosymbiosis spawn new host species?
Debates about the types of heritable elements (nuclear genes versus endosymbionts) that promote eukaryotic species formation have a rich history in evolutionary biology.
Photo of parasitc wasp, Nasonia vitripennis (2mm). This female is infected with Wolbachia that induce a sperm-egg incompatibility called cytoplasmic incompatibility and may act as an insect speciation agent. Photo by Jeremy Brozek, 2004. However, despite efforts to put symbiosis into the mainstream of speciation literature, there has been little evidence that seriously supports endosymbiont-assisted speciation. Studies of Wolbachia, however, are changing this view and the reason is simple — these bacteria are in the business of modifying reproduction, the central element of speciation. The most common reproductive alteration caused by Wolbachia is an incompatibility between eggs and sperm of hosts, termed cytoplasmic incompatibility (CI). It is a post-fertilization incompatibility that typically leads to F1 hybrid inviability in crosses between infected males and uninfected females, or females harboring a different strain of Wolbachia than that in the male. Sperm are modified by the bacteria in the testes and unless the egg carries the same strain, the paternal genome improperly condenses in the fertilized egg and inviability results.
My research interests focus on linking endosymbionts to the incipient, and thus critical, stages of species formation. For example in the parasitic wasp genus Nasonia, our research shows that crossings between infected individuals of all three species produce few to no hybrid offspring, due to Wolbachia-induced CI. Upon curing of the insects by antibiotics, the species are compatible and produce many fertile and viable hybrids, indicating that CI can act as a primary isolating barrier between all three species. Furthermore, in the younger species pair (divergence time ~0.2 Mya), our findings indicate that CI evolved early in the speciation event, prior to the evolution of other hybrid maladies. This study remains one of the first examples of 'infectious speciation', and links endosymbiosis to the first steps of speciation. The finding demonstrates that it is at least plausible for endosymbionts to play a causal role in the origin of species. Such studies will move the controversy on endosymbiont-assisted speciation from whether it occurs, to how important it is. In the long term, I plan to investigate other insect systems for similar evidence and to continue experimental population studies which assess the conditions that restrict or promote endosymbiont-assisted speciation in nature.
Summary: Without endosymbiosis, the biosphere we know today would be nearly unrecognizable. It is my aim to understand the origins, evolution, and impacts of endosymbiosis using population genetic, comparative genomic, and classical genetic methods. Wolbachia is an excellent model system for these challenges because of its lifestyle diversity, unparalleled abundance and distribution, and dramatic effects that it can have on its hosts.