ORCID Profile
0000-0002-7236-7368
Current Organisation
Georgia Institute of Technology
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Publisher: Springer Science and Business Media LLC
Date: 14-09-2011
Abstract: A major goal of molecular evolutionary biology is to understand the fate and consequences of duplicated genes. In this context, aphids are intriguing because the newly sequenced pea aphid genome harbors an extraordinary number of lineage-specific gene duplications relative to other insect genomes. Though many of their duplicated genes may be involved in their complex life cycle, duplications in nutrient amino acid transporters appear to be associated rather with their essential amino acid poor diet and the intracellular symbiosis aphids rely on to compensate for dietary deficits. Past work has shown that some duplicated amino acid transporters are highly expressed in the specialized cells housing the symbionts, including a paralog of an aphid-specific expansion homologous to the Drosophila gene slimfast . Previous data provide evidence that these bacteriocyte-expressed transporters mediate amino acid exchange between aphids and their symbionts. We report that some nutrient amino acid transporters show male-biased expression. Male-biased expression characterizes three paralogs in the aphid-specific slimfast expansion, and the male-biased expression is conserved across two aphid species for at least two paralogs. One of the male-biased paralogs has additionally experienced an accelerated rate of non-synonymous substitutions. This is the first study to document male-biased slimfast expression. Our data suggest that the male-biased aphid slimfast paralogs erged from their ancestral function to fill a functional role in males. Furthermore, our results provide evidence that members of the slimfast expansion are maintained in the aphid genome not only for the previously hypothesized role in mediating amino acid exchange between the symbiotic partners, but also for sex-specific roles.
Publisher: Wiley
Date: 16-02-2014
DOI: 10.1111/MEC.12627
Abstract: Symbiosis is well known to influence bacterial symbiont genome evolution and has recently been shown to shape eukaryotic host genomes. Intriguing patterns of host genome evolution, including remarkable numbers of gene duplications, have been observed in the pea aphid, a sap‐feeding insect that relies on a bacterial endosymbiont for amino acid provisioning. Previously, we proposed that gene duplication has been important for the evolution of symbiosis based on aphid‐specific gene duplication in amino acid transporters ( AAT s), with some paralogs highly expressed in the cells housing symbionts (bacteriocytes). Here, we use a comparative approach to test the role of gene duplication in enabling recruitment of AAT s to bacteriocytes. Using genomic and transcriptomic data, we annotate AAT s from sap‐feeding and non sap‐feeding insects and find that, like aphids, AAT gene families have undergone independent large‐scale gene duplications in three of four additional sap‐feeding insects. RNA ‐seq differential expression data indicate that, like aphids, the sap‐feeding citrus mealybug possesses several lineage‐specific bacteriocyte‐enriched paralogs. Further, differential expression data combined with quantitative PCR support independent evolution of bacteriocyte enrichment in sap‐feeding insect AAT s. Although these data indicate that gene duplication is not necessary to initiate host/symbiont amino acid exchange, they support a role for gene duplication in enabling AAT s to mediate novel host/symbiont interactions broadly in the sap‐feeding suborder Sternorrhyncha. In combination with recent studies on other symbiotic systems, gene duplication is emerging as a general pattern in host genome evolution.
Publisher: Proceedings of the National Academy of Sciences
Date: 23-07-2019
Abstract: Plant sap-feeding insects thrive despite feeding exclusively on a diet lacking in essential amino acids. This nutritional deficit is countered through endosymbiotic relationships with microbial symbionts. Nonessential amino acids, vital for microbial symbionts, are utilized by symbiont metabolic pathways and yield essential amino acids required by their eukaryotic hosts. Symbionts are completely dependent on their host to meet nutritional requirements. The endosymbionts are surrounded in idually by host-derived symbiosomal membranes and are housed within specialized host bacteriocyte cells. The transport capabilities of the symbiosomal membrane remain unknown. Here, we identify a transport system that mediates a crucial step in this metabolic complementarity: a transporter capable of transporting nonessential amino acids across the symbiosomal membrane of the pea aphid Acyrthosiphon pisum .
Publisher: Oxford University Press (OUP)
Date: 24-05-2011
Abstract: In insects, some of the most ecologically important symbioses are nutritional symbioses that provide hosts with novel traits and thereby facilitate exploitation of otherwise inaccessible niches. One such symbiosis is the ancient obligate intracellular symbiosis of aphids with the γ-proteobacteria, Buchnera aphidicola. Although the nutritional basis of the aphid/Buchnera symbiosis is well understood, the processes and structures that mediate the intimate interactions of symbiotic partners remain uncharacterized. Here, using a de novo approach, we characterize the complement of 40 amino acid polyamine organocation (APC) superfamily member amino acid transporters (AATs) encoded in the genome of the pea aphid, Acyrthosiphon pisum. We find that the A. pisum APC superfamily is characterized by extensive gene duplications such that A. pisum has more APC superfamily transporters than other fully sequenced insects, including a ten paralog aphid-specific expansion of the APC transporter slimfast. Detailed expression analysis of 17 transporters selected on the basis of their phylogenetic relationship to five AATs identified in an earlier bacteriocyte expressed sequence tag study distinguished a subset of eight transporters that have been recruited for amino acid transport in bacteriocyte cells at the symbiotic interface. These eight transporters include transporters that are highly expressed and/or highly enriched in bacteriocytes and intriguingly, the four AATs that show bacteriocyte-enriched expression are all members of gene family expansions, whereas three of the four that are highly expressed but not enriched in bacteriocytes retain one-to-one orthology with transporters in other genomes. Finally, analysis of evolutionary rates within the large A. pisum slimfast expansion demonstrated increased rates of molecular evolution coinciding with two major shifts in expression: 1) a loss of gut expression and possibly a gain of bacteriocyte expression and 2) loss of expression in all surveyed tissues in asexual females. Taken together, our characterization of nutrient AATs at the aphid/Buchnera symbiotic interface provides the first examination of the processes and structures operating at the interface of an obligate intracellular insect nutritional symbiosis, offering unique insight into the types of genomic change that likely facilitated evolutionary maintenance of the symbiosis.
Publisher: Proceedings of the National Academy of Sciences
Date: 16-10-2023
Publisher: Proceedings of the National Academy of Sciences
Date: 26-05-2015
Abstract: The role of symbiosis in bacterial symbiont genome evolution is well understood, yet the ways that symbiosis shapes host genomes or more particularly, host/symbiont genome coevolution in the holobiont is only now being revealed. Here, we identify three coevolutionary signatures that characterize holobiont genomes. The first signature, host/symbiont collaboration, arises when completion of essential pathways requires host/endosymbiont genome complementarity. Metabolic collaboration has evolved numerous times in the pathways of amino acid and vitamin biosynthesis. Here, we highlight collaboration in branched-chain amino acid and pantothenate (vitamin B5) biosynthesis. The second coevolutionary signature is acquisition, referring to the observation that holobiont genomes acquire novel genetic material through various means, including gene duplication, lateral gene transfer from bacteria that are not their current obligate symbionts, and full or partial endosymbiont replacement. The third signature, constraint, introduces the idea that holobiont genome evolution is constrained by the processes governing symbiont genome evolution. In addition, we propose that collaboration is constrained by the expression profile of the cell lineage from which endosymbiont-containing host cells, called bacteriocytes, are derived. In particular, we propose that such differences in bacteriocyte cell lineage may explain differences in patterns of host/endosymbiont metabolic collaboration between the sap-feeding suborders Sternorrhyncha and Auchenorrhynca. Finally, we review recent studies at the frontier of symbiosis research that are applying functional genomic approaches to characterization of the developmental and cellular mechanisms of host/endosymbiont integration, work that heralds a new era in symbiosis research.
Publisher: Springer Science and Business Media LLC
Date: 25-03-2015
Publisher: Oxford University Press (OUP)
Date: 15-02-2016
DOI: 10.1093/GBE/EVW020
Publisher: Elsevier BV
Date: 06-2013
DOI: 10.1016/J.CELL.2013.05.040
Abstract: The smallest reported bacterial genome belongs to Tremblaya princeps, a symbiont of Planococcus citri mealybugs (PCIT). Tremblaya PCIT not only has a 139 kb genome, but possesses its own bacterial endosymbiont, Moranella endobia. Genome and transcriptome sequencing, including genome sequencing from a Tremblaya lineage lacking intracellular bacteria, reveals that the extreme genomic degeneracy of Tremblaya PCIT likely resulted from acquiring Moranella as an endosymbiont. In addition, at least 22 expressed horizontally transferred genes from multiple erse bacteria to the mealybug genome likely complement missing symbiont genes. However, none of these horizontally transferred genes are from Tremblaya, showing that genome reduction in this symbiont has not been enabled by gene transfer to the host nucleus. Our results thus indicate that the functioning of this three-way symbiosis is dependent on genes from at least six lineages of organisms and reveal a path to intimate endosymbiosis distinct from that followed by organelles.
Location: United States of America
No related grants have been discovered for Rebecca Duncan.