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Convergent evolution of metabolic roles in bacterial co-symbionts of insects.

ABSTRACT: A strictly host-dependent lifestyle has profound evolutionary consequences for bacterial genomes. Most prominent is a sometimes-dramatic amount of gene loss and genome reduction. Recently, highly reduced genomes from the co-resident intracellular symbionts of sharpshooters were shown to exhibit a striking level of metabolic interdependence. One symbiont, called Sulcia muelleri (Bacteroidetes), can produce eight of the 10 essential amino acids, despite having a genome of only 245 kb. The other, Baumannia cicadellinicola (gamma-Proteobacteria), can produce the remaining two essential amino acids as well as many vitamins. Cicadas also contain the symbiont Sulcia, but lack Baumannia and instead contain the co-resident symbiont Hodgkinia cicadicola (alpha-Proteobacteria). Here we report that, despite at least 200 million years of divergence, the two Sulcia genomes have nearly identical gene content and gene order. Additionally, we show that despite being phylogenetically distant and drastically different in genome size and architecture, Hodgkinia and Baumannia have converged on gene sets conferring similar capabilities for essential amino acid biosynthesis, in both cases precisely complementary to the pathways conserved in Sulcia. In contrast, they have completely divergent capabilities for vitamin biosynthesis. Despite having the smallest gene set known in bacteria, Hodgkinia devotes at least 7% of its proteome to cobalamin (vitamin B(12)) biosynthesis, a significant metabolic burden. The presence of these genes can be explained by Hodgkinia's retention of the cobalamin-dependent version of methionine synthase instead of the cobalamin-independent version found in Baumannia, a situation that necessitates retention of cobalamin biosynthetic capabilities to make the essential amino acid methionine.

SUBMITTER: McCutcheon JP

PROVIDER: S-EPMC2741262 | biostudies-literature | 2009 Sep

REPOSITORIES: biostudies-literature

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Convergent evolution of metabolic roles in bacterial co-symbionts of insects.

McCutcheon John P JP McDonald Bradon R BR Moran Nancy A NA

Proceedings of the National Academy of Sciences of the United States of America 20090824 36

A strictly host-dependent lifestyle has profound evolutionary consequences for bacterial genomes. Most prominent is a sometimes-dramatic amount of gene loss and genome reduction. Recently, highly reduced genomes from the co-resident intracellular symbionts of sharpshooters were shown to exhibit a striking level of metabolic interdependence. One symbiont, called Sulcia muelleri (Bacteroidetes), can produce eight of the 10 essential amino acids, despite having a genome of only 245 kb. The other, B ...[more]

PMID: 19706397

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Project description:Genome reduction in obligately intracellular bacteria is one of the most well-established patterns in the field of molecular evolution. In the extreme, many sap-feeding insects harbor nutritional symbionts with genomes that are so reduced that it is not clear how they perform basic cellular functions. For example, the primary symbiont of psyllids (Carsonella) maintains one of the smallest and most AT-rich bacterial genomes ever identified and has surprisingly lost many genes that are thought to be essential for its role in provisioning its host with amino acids. However, our understanding of this extreme case of genome reduction is limited, as genomic data for Carsonella are available from only a single host species, and little is known about the functional role of "secondary" bacterial symbionts in psyllids. To address these limitations, we analyzed complete Carsonella genomes from pairs of congeneric hosts in three divergent genera within the Psyllidae (Ctenarytaina, Heteropsylla, and Pachypsylla) as well as complete secondary symbiont genomes from two of these host species (Ctenarytaina eucalypti and Heteropsylla cubana). Although the Carsonella genomes are generally conserved in size, structure, and GC content and exhibit genome-wide signatures of purifying selection, we found that gene loss has remained active since the divergence of the host species and had a particularly large impact on the amino acid biosynthesis pathways that define the symbiotic role of Carsonella. In some cases, the presence of additional bacterial symbionts may compensate for gene loss in Carsonella, as functional gene content indicates a high degree of metabolic complementarity between co-occurring symbionts. The genomes of the secondary symbionts also show signatures of long-term evolution as vertically transmitted, intracellular bacteria, including more extensive genome reduction than typically observed in facultative symbionts. Therefore, a history of co-evolution with secondary bacterial symbionts can partially explain the ongoing genome reduction in Carsonella. However, the absence of these secondary symbionts in other host lineages indicates that the relationships are dynamic and that other mechanisms, such as changes in host diet or functional coordination with the host genome, must also be at play.

Project description:UNLABELLED:The ability to cultivate food is an innovation that has produced some of the most successful ecological strategies on the planet. Although most well recognized in humans, where agriculture represents a defining feature of civilization, species of ants, beetles, and termites have also independently evolved symbioses with fungi that they cultivate for food. Despite occurring across divergent insect and fungal lineages, the fungivorous niches of these insects are remarkably similar, indicating convergent evolution toward this successful ecological strategy. Here, we characterize the microbiota of ants, beetles, and termites engaged in nutritional symbioses with fungi to define the bacterial groups associated with these prominent herbivores and forest pests. Using culture-independent techniques and the in silico reconstruction of 37 composite genomes of dominant community members, we demonstrate that different insect-fungal symbioses that collectively shape ecosystems worldwide have highly similar bacterial microbiotas comprised primarily of the genera Enterobacter, Rahnella, and Pseudomonas. Although these symbioses span three orders of insects and two phyla of fungi, we show that they are associated with bacteria sharing high whole-genome nucleotide identity. Due to the fine-scale correspondence of the bacterial microbiotas of insects engaged in fungal symbioses, our findings indicate that this represents an example of convergence of entire host-microbe complexes. IMPORTANCE:The cultivation of fungi for food is a behavior that has evolved independently in ants, beetles, and termites and has enabled many species of these insects to become ecologically important and widely distributed herbivores and forest pests. Although the primary fungal cultivars of these insects have been studied for decades, comparatively little is known of their bacterial microbiota. In this study, we show that diverse fungus-growing insects are associated with a common bacterial community composed of the same dominant members. Furthermore, by demonstrating that many of these bacteria have high whole-genome similarity across distantly related insect hosts that reside thousands of miles apart, we show that these bacteria are an important and underappreciated feature of diverse fungus-growing insects. Because of the similarities in the agricultural lifestyles of these insects, this is an example of convergence between both the life histories of the host insects and their symbiotic microbiota.

Project description:The mosquito microbiota is composed of several lineages of microorganisms whose ecological roles and evolutionary histories have yet to be investigated in depth. Among these microorganisms, Asaia bacteria play a prominent role, given their abundance in the gut, reproductive organs, and salivary glands of different mosquito species, while their presence has also been reported in several other insects. Notably, Asaia has great potential as a tool for the control of mosquito-borne diseases. Here, we present a wide phylogenomic analysis of Asaia strains isolated from different species of mosquito vectors and from different populations of the Mediterranean fruit fly (medfly), Ceratitis capitata, an insect pest of worldwide economic importance. We show that phylogenetically distant lineages of Asaia experienced independent genome reductions, despite following a common pattern, characterized by the early loss of genes involved in genome stability. This result highlights the role of specific metabolic pathways in the symbiotic relationship between Asaia and the insect host. Finally, we discovered that all but one of the Asaia strains included in the study possess the pyrethroid hydrolase gene. Phylogenetic analysis revealed that this gene is ancestral in Asaia, strongly suggesting that it played a role in the establishment of the symbiotic association between these bacteria and the mosquito hosts. We propose that this gene from the symbiont contributed to initial pyrethroid resistance in insects harboring Asaia, also considering the widespread production of pyrethrins by several plants.IMPORTANCE We have studied genome reduction within several strains of the insect symbiont Asaia isolated from different species/strains of mosquito and medfly. Phylogenetically distant strains of Asaia, despite following a common pattern involving the loss of genes related to genome stability, have undergone independent genome reductions, highlighting the peculiar role of specific metabolic pathways in the symbiotic relationship between Asaia and its host. We also show that the pyrethroid hydrolase gene is present in all the Asaia strains isolated except for the South American malaria vector Anopheles darlingi, for which resistance to pyrethroids has never been reported, suggesting a possible involvement of Asaia in determining resistance to insecticides.

Dataset Information

Convergent evolution of metabolic roles in bacterial co-symbionts of insects.

Publications

Convergent evolution of metabolic roles in bacterial co-symbionts of insects.

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