Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 112, Issue 33, Pages 10255-10261Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.1423305112
Keywords
symbiosis; insect nutritional; coevolution; amino acid biosynthesis; vitamin biosynthesis
Categories
Funding
- National Science Foundation Awards [IOS-1121847, IOS-1354154]
- Graduate Research Fellowship [DG1E-0951782]
- [DEB-1406631]
- Direct For Biological Sciences
- Division Of Integrative Organismal Systems [1354154] Funding Source: National Science Foundation
- Division Of Environmental Biology
- Direct For Biological Sciences [1406631] Funding Source: National Science Foundation
- Division Of Integrative Organismal Systems
- Direct For Biological Sciences [1121847] Funding Source: National Science Foundation
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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.
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