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Bacterial Endosymbionts in Animals Nancy a Moran* and Paul Baumann†

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Bacterial Endosymbionts in Animals Nancy a Moran* and Paul Baumann† 270 Bacterial endosymbionts in animals Nancy A Moran* and Paul Baumann† Molecular phylogenetic studies reveal that many This review is concentrated on evolutionary aspects of endosymbioses between bacteria and invertebrate hosts result endosymbiosis involving bacteriocyte associates of animals. from ancient infections followed by strict vertical transmission For these bacteria, there is clear evidence of a coevolved, within host lineages. Endosymbionts display a distinctive mutualistic relationship with the host and a distinctive set constellation of genetic properties including AT-biased base of genetic traits that result from the association. To date, composition, accelerated sequence evolution, and, at least most studies have focused on insect symbionts, although sometimes, small genome size; these features suggest there are a few evolutionary studies of symbionts in other increased genetic drift. Molecular genetic characterization also invertebrate groups. The best-characterized animal has revealed adaptive, host-beneficial traits such as endosymbiont is Buchnera aphidicola, a bacteriocyte-associ- amplification of genes underlying nutrient provision. ated mutualist of aphids, insects that feed on phloem sap of host plants. Many comparative studies of host-beneficial Addresses and other loci have been carried out using Buchnera, and a *Department of Ecology and Evolutionary Biology, University of full genome has recently been completely sequenced Arizona, Tucson, Arizona 85721, USA; e-mail: [email protected] (H Ishikawa, personal communication), with sequencing of † Microbiology Section, University of California at Davis, Davis, another genome in progress. We emphasize molecular stud- California 95616, USA; e-mail: [email protected] ies within the past two years that have applied molecular Current Opinion in Microbiology 2000, 3:270–275 approaches to reconstruct the evolution of Buchnera and 1369-5274/00/$ — see front matter other bacteriocyte-associates. © 2000 Elsevier Science Ltd. All rights reserved. Molecular phylogenetics and co-speciation Introduction Although Buchner [1] speculated about the age and origin In recent years, technological advances allowing molecular of endosymbioses, no firm information about this topic was phylogenetic characterization have enabled exploration of possible for noncultivable symbionts before DNA the world of bacteria that cannot be cultured — a category sequencing became feasible. The first such studies were that includes the majority of life forms. Among the non- on Buchnera, for which phylogenetic analyses have now cultivable bacteria about which we have discovered most revealed matching between phylogenies of symbionts and are the endosymbionts that live in animal cells and are aphid hosts over a variety of evolutionary time scales. This transmitted vertically at the time of host reproduction. congruence between host and symbiont phylogenetic trees Although common in many invertebrates, intracellular bac- implies co-speciation and synchronous diversification. terial associates of animals were little studied until about Initial studies, for distantly related aphids and their 10 years ago. A large portion of what was known was com- Buchnera associates, supported vertical transmission down piled in a book by Paul Buchner [1], which remains the host lineages from the time of the common ancestor of central reference for information on the diversity and dis- aphids, which is estimated to be some 150–250 million tribution of endosymbionts. One of the most intriguing years ago on the basis of dating from host fossils [3•]. aspects of these endosymbioses concerns their evolution- Recently, phylogenetic congruence has been shown for ary origins and adaptive modifications. Buchnera of closely related aphids that interact ecologically [4]. Analyses of intraspecific polymorphisms in aphid mito- The bacteria that inhabit animal cells can be divided into chondrial and Buchnera markers suggest that horizontal several groups. The most distinctive are ‘primary’ sym- transfer is absent even within a single aphid species [5]. bionts that reside within specialized host cells called Thus, maternal transmission appears to be the sole mech- bacteriocytes. They have reciprocally beneficial — often anism of infection. An implication of these results for reciprocally obligate — relationships with hosts and occur bacterial population structure is that no genetic recombi- in many terrestrial arthropods as well as some marine nation between strains of bacteria from different aphids invertebrates. ‘Secondary’ symbionts and intracellular has occurred. pathogens are more sporadically associated with host indi- viduals and vary in tissues occupied. Because effects on Phylogenetic congruence with hosts, implying co-speciation, hosts are usually unknown, there is no clear demarcation also has been reported for other bacteriocyte-associates, between symbionts and pathogens: a wide range of inter- including symbionts of tsetse flies [6•], cockroaches [7], cer- actions certainly exist between non-bacteriocyte associates tain marine bivalves [8•], carpenter ants [9•], and the and their hosts (for example see [2•]). Infection of hosts Wolbachia pipientis that appear to be mutualistic in nematodes can be strictly maternal, maternal with occasional horizon- [10•]. All of these studies span ancient divergences among tal transfer, or entirely horizontal, and there is no absolute taxa, indicating that, in each case, a single ancient infection correspondence between mode of transmission and effects was followed by co-speciation across millions of years, with on host fitness. symbiotic bacteria diverging in parallel with their hosts. Bacterial endosymbionts Moran and Baumann 271 Although there is probably some association between symbiotic adaptations that benefit the hosts. Most animal maternal transmission as the primary route of infection and symbionts contribute rare nutrients that the host itself can- congruent of host and symbiont phylogenies spanning evo- not make. The biosynthetic contributions of symbionts lutionary time periods, either may exist without the other. have been explored in several systems, including Buchnera Some secondary symbionts and intracellular pathogens in [26–28], through experiments using symbiotic and artifi- insects are transmitted maternally but nonetheless under- cially cured hosts. In addition, studies of enzymatic activity go occasional horizontal transmission, through an unknown or end product synthesis by symbionts have been used to route, as implied by molecular studies of Wolbachia pipien- document metabolic contributions, such as sulfur oxida- tis [11,12] and secondary symbionts of aphids [13] and tion and assimilation of inorganic nitrogen and carbon in tsetse flies [7]. Conversely, some symbionts undergo co- symbionts of marine hosts (for example [29•,30,31]). speciation with hosts in the absence of maternal Metabolic studies in intact symbionts have recently been transmission. This situation appears to characterize Vibrio complemented and extended by molecular characteriza- fischeri, which colonize the light organs of squids [14]; these tion of genes involved in relevant pathways (for example symbionts exist in sea water and reinfect juveniles each [17••,32,33•,34,35]). The retention of symbiont loci under- generation but show phylogenetic congruence with hosts lying a particular metabolic pathway is strong evidence for and adaptation to their own host lineage in experimental a contribution to host metabolism, since bacterial lineages transfers [15•]. Symbionts of other marine invertebrates, routinely lose genes not used [36]. such as hydrothermal vent tube worms, lack both maternal transmission and phylogenetic congruence with hosts [16]. Plasmid-borne biosynthetic genes and gene amplification Molecular phylogenetic analyses also reveal the relation- The molecular basis of symbiont adaptations for providing ships of endosymbionts to other groups of bacteria [3•]. nutrients to their hosts is best studied in Buchnera. Plant Several, including the associates of aphids [17••], tsetse phloem sap is deficient in essential amino acids, and flies [6•], psyllids [18•], ants [19] and some bivalves [8•,20], Buchnera provides several of these to aphid hosts [17••]. are related to the enteric bacteria, within the Despite its small genome, Buchnera retains genes for γ-Proteobacteria. Other groups of bacteria have also given biosynthesis of several amino acids that the hosts are rise to endosymbionts, such as the Flavobacteria in cock- unable to produce for themselves. Furthermore, in many roaches [7]. Among the γ-Proteobacteria, endosymbionts of Buchnera lineages, genes underlying the rate-limiting step different host groups have evolved as independent lin- of tryptophan biosynthesis (trpEG) and genes underlying eages from nonsymbiotic bacteria [3•]. leucine biosynthesis (leuABCD) have been recruited to plasmids [17••]. The leu plasmid is of the IncFII group The precise phylogenetic relationships of endosymbiotic first isolated from Salmonella and bears, in addition to repA bacteria are often uncertain, because of limited information genes characteristic of those plasmids, a single copy of in the 16S rRNA gene (the primary sequence used for phy- leuABCD, whereas the trpEG plasmid bears tandem repeats logenetic characterization) and also the elevated base of a unit containing trpEG [17••]. In each case, the plasmid substitution rates and base compositional biases typical of location
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