Signatures of Host/Symbiont Genome Coevolution in Insect Nutritional
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PAPER Signatures of host/symbiont genome coevolution in COLLOQUIUM insect nutritional endosymbioses Alex C. C. Wilson1 and Rebecca P. Duncan Department of Biology, University of Miami, Coral Gables, FL 33146 Edited by John P. McCutcheon, University of Montana, Missoula, MT, and accepted by the Editorial Board May 5, 2015 (received for review February 2, 2015) The role of symbiosis in bacterial symbiont genome evolution is these ancient, intimate symbiotic associations. Our purpose here well understood, yet the ways that symbiosis shapes host genomes is to highlight three signatures of genome coevolution across or more particularly, host/symbiont genome coevolution in the available holobiont genomes and to draw attention to work at holobiont is only now being revealed. Here, we identify three the frontier of symbiosis research that elucidates mechanisms of coevolutionary signatures that characterize holobiont genomes. The holobiont regulation and integration. first signature, host/symbiont collaboration, arises when completion of essential pathways requires host/endosymbiont genome com- Three Signatures: Collaboration, Acquisition, and Constraint plementarity. Metabolic collaboration has evolved numerous times Holobiont genome evolution is characterized by patterns of col- in the pathways of amino acid and vitamin biosynthesis. Here, we laboration, acquisition, and constraint. Coevolution typically fea- highlight collaboration in branched-chain amino acid and pantothe- tures host/endosymbiont collaboration on completion of critical nate (vitamin B5) biosynthesis. The second coevolutionary signature metabolic pathways—a set of pathways that is similar across taxa, is acquisition, referring to the observation that holobiont genomes apparently constrained by eukaryotic host gene repertoire and yet, acquire novel genetic material through various means, including concurrently, holobiont genome evolution is dynamic. Dynamic gene duplication, lateral gene transfer from bacteria that are not features include acquisition of novel genomic material like du- their current obligate symbionts, and full or partial endosymbiont plicate genes, genes acquired by lateral gene transfer that enhance replacement. The third signature, constraint, introduces the idea collaboration, and acquisition of coprimary symbionts or even new that holobiont genome evolution is constrained by the processes primary symbionts by symbiont replacement. EVOLUTION governing symbiont genome evolution. In addition, we propose that collaboration is constrained by the expression profile of the Collaboration cell lineage from which endosymbiont-containing host cells, called Long before it was possible to elucidate the metabolic repertoire bacteriocytes, are derived. In particular, we propose that such of an organism by sequencing its DNA, researchers established differences in bacteriocyte cell lineage may explain differences in the metabolic basis of many insect nutritional symbioses experi- patterns of host/endosymbiont metabolic collaboration between mentally by quantifying the growth and fecundity of insects ma- the sap-feeding suborders Sternorrhyncha and Auchenorrhynca. nipulated in a diversity of ways that included some combination of Finally, we review recent studies at the frontier of symbiosis research endosymbiont removal and diet manipulations (13). Such analyses that are applying functional genomic approaches to characterization established that endosymbionts provision host insects with dietary of the developmental and cellular mechanisms of host/endosymbiont components lacking or at low availability in their diets. Thus, at integration, work that heralds a new era in symbiosis research. the beginning of the genomic revolution it was understood that hosts supply endosymbionts with metabolic precursors that en- symbiosis | insect nutritional | coevolution | amino acid biosynthesis | dosymbionts metabolically transform into host-required dietary vitamin biosynthesis components. Notably, from an organismal perspective, insect nu- tritional symbioses in pregenome times were partnerships between any insects have established persistent, intimate associa- two discrete organisms: the host and the endosymbiont. Endo- Mtions with vertically transmitted microbial symbionts. These symbiont whole-genome sequencing affirmed and continues to ancient, commonly intracellular symbionts are, owing to their affirm the nutritional role played by symbionts, whereas host greatly reduced, gene-poor genomes, uncultivable outside their genome and transcriptome sequencing reveals a complex por- hosts. Although the whole-genome sequences of obligate insect trait of the nature and extent of host/endosymbiont metabolic endosymbionts continue to yield novel insight into genome evo- complementarity. lution following adoption of an obligate intracellular lifestyle (e.g., Currently the most well-documented examples of host/endo- ref. 1), it is the recent partnering of these symbiont genome se- symbiont metabolic collaboration involve the biosynthesis of quences with those of their insect hosts that fundamentally shifts essential amino acids in plant sap-feeding insects (2, 7–9, 14–16). conceptualization of “the organism,” propelling us into a new era In most cases, holobiont metabolism has been reconstructed in symbiosis research. using the whole-genome sequence of the symbiont coupled with The first paired insect host/endosymbiont genome available a host bacteriome transcriptome (the bacteriome is the host was that of the pea aphid, Acyrthosiphon pisum and its bacterial endosymbiont, Buchnera aphidicola (2, 3). The second was that of the human body louse, Pediculus humanus humanus and its This paper results from the Arthur M. Sackler Colloquium of the National Academy of primary bacterial endosymbiont Candidatus Riesia pediculicola Sciences, “Symbioses Becoming Permanent: The Origins and Evolutionary Trajectories of (4), quickly followed by the carpenter ant, Camponotus floridanus Organelles,” held October 15–17, 2014, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, CA. The complete program (5) and its endosymbiont Candidatus Blochmannia floridanus (6). and video recordings of most presentations are available on the NAS website at www. Other insect holobiont genomes now include the citrus mealybug, nasonline.org/Symbioses. Planococcus citri with its dual endosymbionts (7, 8); the hackberry Author contributions: A.C.C.W. and R.P.D. designed research, performed research, ana- petiole gall psyllid Pachypsylla venusta with its endosymbiont lyzed data, and wrote the paper. Candidatus Carsonella ruddii (9); and the tsetse fly, Glossina The authors declare no conflict of interest. morsitans (10) with its endosymbiont Wigglesworthia glossinidia This article is a PNAS Direct Submission. J.P.M. is a guest editor invited by the Editorial (11, 12). This recent accumulation of holobiont genomes facili- Board. tates elucidation of the patterns that characterize coevolution in 1To whom correspondence should be addressed. Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1423305112 PNAS | August 18, 2015 | vol. 112 | no. 33 | 10255–10261 Downloaded by guest on September 28, 2021 symbiosomal membrane bacteriocyte cell membrane Symbiont with host Bacteriocyte Bacteriome Host insect symbiosomal membrane with symbionts with bacteriocytes with bacteriome Fig. 1. Organization of endosymbionts in insect hosts. Typically enveloped by a host membrane (green) within the cytoplasm of specialized host bacteriocyte cells, insect nutritional endosymbionts (purple) are maternally transmitted and integrated into host development by currently unknown mechanisms. In- dividual bacteriocyte cells house thousands to tens of thousands of symbionts. Many bacteriocyte cells aggregate to form an organ called the bacteriome. Bacteriomes are typically paired and relatively large. organ composed of host bacteriocyte cells that house the en- encoding pantothenate synthetase (E.C. 6.3.2.1) that functions dosymbionts) (Fig. 1) and a partial host genome. In the case of only in pantothenate biosynthesis (Fig. 2) (18). Thus, we venture the pea aphid, metabolic reconstruction leveraged the com- that examination of the host genomes and transcriptomes of plete genome of both symbiont and host (2, 14). The many these four endosymbionts will demonstrate that pantothenate similarities and differences in the collaborative amino acid bio- biosynthesis is indeed functional in these holobionts as a result of synthesis of plant sap-feeding holobionts have recently been host/endosymbiont metabolic collaboration. reviewed by Sloan et al. (9) and Hansen and Moran (17). It is clear that metabolic collaboration is a fundamental sig- Therefore, here we illustrate the collaborative signature of host/ nature of host/symbiont genome coevolution. However, the ex- symbiont genome coevolution by drawing attention to one set of tent to which patterns of metabolic collaboration in holobionts amino acid biosynthesis pathways, those for biosynthesis of the result from convergence and not shared ancestry remains to be branched-chain amino acids. Biosynthesis of the branched-chain determined. Distinguishing between traits shared by conver- amino acids, isoleucine, leucine, and valine, involves host/endo- gence and those shared by common ancestry requires charac- symbiont metabolic collaboration in both A. pisum (14, 15, 16) and ter state information for a broad range of closely related taxa