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The Evolutionary History of Symbiotic Associations Among Bacteria and Their Animal Hosts: a Model

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The Evolutionary History of Symbiotic Associations Among Bacteria and Their Animal Hosts: a Model REVIEW 10.1111/j.1469-0691.2008.02689.x The evolutionary history of symbiotic associations among bacteria and their animal hosts: a model A. Moya1,2, R. Gil1,2 and A. Latorre1,2 1) Institut Cavanilles de Biodiversitat i Biologia Evolutiva and Departament de Gene`tica, Universitat de Vale`ncia, Vale`ncia and 2) CIBER en Epidemiologı´ay Salud Pu´blica (CIBERESP), Spain Abstract A model to explain the evolutionary history of animal-bacteria obligatory mutualistic symbiosis is presented. Dispensability of genes and genetic isolation are key factors in the reduction process of these bacterial genomes. Major steps in such genome reductive evolution, leading towards primary endosimbiosis, and the possibility of complementation or replacement by a secondary symbiont are also indi- cated. Yet, we need to understand what happens at the beginning of the adaptative process towards an obligate mutualistic relationship. For this purpose, we propose to sequence the complete genome of SOPE, the primary endosymbiont of the rice weevil. Keywords: Complementation, endosymbiosis, genome reduction, replacement, SOPE (Sitophilus oryzae primary endorsement) Clin Microbiol Infect 2009; 15 (Suppl.1): 11–13 towards the establishment of an obligate endosymbiosis Corresponding author and reprint requests: A. Moya, Institut occurs when a free-living bacterium infects a host. From this Cavanilles de Biodiversitat i Biologia Evolutiva and Departament de Gene`tica, Universitat de Vale`ncia, Apartado Postal 22085, 46071 Val- point, both organisms co-evolve to adapt to the new e`ncia, Spain situation. The host develops specialized cells to harbour the E-mail: [email protected] bacterium, which, in turn, provides essential nutrients. In this new stable situation, the bacterium suffers an evolutionary genome reductive process (see next section). Eventually, a second bacterial species might join the consortium. Although, initially, this new association might be facultative, if the The establishment of symbiosis among second bacterium provides benefits to the association, a new bacteria and their animal hosts stable association can appear and both bacteria will subse- quently co-evolve. As the reductive process continues, and Many bacteria maintain symbiotic associations with eukary- new genes are rendered unnecessary owing to redundancy, otic cells; this association can be mutualistic, commensal, or two possible outcomes can occur. Either both bacteria will parasitic. In some cases, the relationship is so close that the be needed to keep a healthy consortium (complementation) bacteria live inside the host cell, an association called endo- or, depending upon which genome is affected by the loss of symbiosis. genes needed for the synthesis of molecules essential for the Bacterial endosymbioses are widespread among higher life association, one bacterium can begin an extreme degenera- forms. Insects have been particularly well studied, where the tive process, which may end with its extinction; in this case, establishment of symbiotic associations with bacteria has the retained bacterium will continue the reductive process allowed them to grow on imbalanced food resources (e.g. alone (replacement). plant sap, cereals, or blood), poor in essential nutrients but with the nutrients being provided by the bacteria [1,2]. The Factors affecting the process of genome symbiotic bacteria reside in specialized host cells called reduction bacteriocytes, and are vertically transmitted from the mother to the offspring. Transition to an obligate intracellular lifestyle in bacteria triggers a cascade of changes that shape As a consequence of their access to an intracellular environ- the genome structure and content, leading to a reduction in ment, free-living bacteria alter their genome composition, genome size and an increase in the A + T content, among sometimes in a dramatic way. Within a protected and stable other features. Fig. 1 shows a model for the establishment environment, many genes are rendered unnecessary, and evolution of symbiotic associations. The first step whereas others become redundant because their functions ª2009 The Authors Journal Compilation ª2009 European Society of Clinical Microbiology and Infectious Diseases 12 Clinical Microbiology and Infection, Volume 15, Supplement 1, January 2009 CMI Replacement 6 Animal 5 1 2 4 7 3 Bacterium Fig. 1. Major steps in the evolution of Complementation endosymbiosis. See text for more details. can be supplied by the host. As a consequence, genetic mate- Empirical evidence from insect rial can be lost without a detrimental effect and can accumu- endosymbiosis late mutations because of the lack of natural selection to purge them. In addition, as compared to the high numbers of free-living bacteria in adult hosts, relatively few endos- Fig. 2 shows most of the bacterial insect endosymbionts that ymbionts are maternally inherited by the offspring of the have been analysed, the majority of them belonging to the host. Thus, such systematic bottlenecking over generations c-proteobacteria. They can be regarded as primary endo- favours the action of random drift [3]. Another consequence symbionts (essential for its host fitness and survival) or of living in an intracellular environment is that bacterial secondary endosymbionts (when they are facultative or can endosymbionts remain relatively isolated, which favours the live outside of the eukaryotic cells). lack of horizontal gene transfer and DNA intake [4]. To We are interested in studying the evolution of these summarize, dispensability of highly mutated and non-essential genomes to identify which changes occur during their adapta- genes, and genetic isolation, are key features in the process tion to intracellular life and the processes that cause them, of genome reduction. as well as to determine factors involved in establishing a Bacterium Genome (kb) Living style Host Buchnera aphidicola BCc 422 P Aphids Buchnera aphidicola BBp 618 P Aphids Buchnera aphidicola BSg 641 P Aphids Buchnera aphidicola BAp 640 P Aphids Blochmannia floridanus * 705 P Carpenter ants Wigglesworthia glossinidia 697 P Tse-tse flies γ-Proteobacteria SOPE ~ 3000 P Rice weevils Fig. 2. Bacterial symbioses among insects. Sodalis glosinidius 4171 S Tse-tse flies Phylogenetic relationships among the main Hamiltonella defensa * S Aphids and whiteflies bacterial symbionts of insects that have been E. coli 4000 – 5594 F analysed are shown. Species whose genomes Salmonella enterica 3600 - 8000 F have been completely sequenced appear in Carsonella ruddii * 160 P Psyllids bold. Free-living relatives appear in grey. P, Portiera aleyrodidarum * P Whiteflies primary endosymbiont; S, secondary symbiont; β-Proteobacteria Tremblaya princeps * P Mealybugs Flavobacterium- F, free-living. *The species name is under the Blattabacterium sp. P Cockroaches and Bacteroides termites category Candidatus. ª2009 The Authors Journal Compilation ª2009 European Society of Clinical Microbiology and Infectious Diseases, CMI, 15 (Suppl. 1), 11–13 CMI Moya et al. Evolution of animal-bacteria symbioses 13 mutualistic relationship instead of a pathogenic one. The genomes of these two bacteria will allow us to determine sequencing of genomes from bacteria with young and old which genes are lost at the beginning of the adaptive process, endosymbiotic relationships with their eukaryotic hosts will and to draw some conclusions about the process of adaptation assist in that task. All the primary endosymbionts analysed of bacteria to endosymbiotic life. so far have genome sizes about eight to ten times smaller than their free-living relatives. One of the most extreme Transparency Declaration cases, that of Buchnera aphidicola from the aphid Cinara cedri (BCc strain), has recently been sequenced in our laboratory and might represent a final stage in the endosymbiotic rela- Financial support was provided by projects BFU2006-06003 tionship [5]. In all previous cases analysed, B. aphidicola from Ministerio de Educacio´n y Ciencia (MEC), Spain, to A. provides essential amino acids plus riboflavin to the aphid Latorre and GV/2007/050 from Generalitat Valenciana, Spain, host. However, B. aphidicola BCc has lost the ability to syn- to R. Gil. R. Gil was a recipient of a contract in the ‘Ramo´n thesize tryptophan and riboflavin, and most retained genes y Cajal’ Program from the MEC, Spain. The author declares are evolving at a faster rate [5]. In addition, another endo- no conflicts of interest. symbiont, Serratia symbiotica, has been found in all analysed cedar aphid populations. On the basis of all these findings, References we postulate that B. aphidicola BCc is losing its symbiotic capacity and is being complemented (and might be replaced) by the highly abundant coexisting S. symbiotica. 1. Douglas AE. Nutritional interactions in insect–microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 1998; To better understand the molecular and evolutionary basis 43: 17–37. of symbiosis, it is necessary to sequence and characterize the 2. Baumann P. Biology bacteriocyte-associated endosymbionts of plant genome of a bacterium in the first stages of the process. For sap-sucking insects. Annu Rev Microbiol 2005; 59: 155–189. this purpose, we chose SOPE, the primary endosymbiont of 3. Moran NA. Accelerated evolution and Muller’s rachet in endosymbi- otic bacteria. Proc Natl Acad Sci USA 1996; 93: 2873–2878. c the rice weevil, Sitophilus oryzae. SOPE is a -proteobacterium 4. Silva FJ, Latorre A, Moya A. Why are the genomes of endosymbiotic
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