Dataset Information

Bacterial endosymbiosis in a chordate host: long-term co-evolution and conservation of secondary metabolism.

ABSTRACT: Intracellular symbiosis is known to be widespread in insects, but there are few described examples in other types of host. These symbionts carry out useful activities such as synthesizing nutrients and conferring resistance against adverse events such as parasitism. Such symbionts persist through host speciation events, being passed down through vertical transmission. Due to various evolutionary forces, symbionts go through a process of genome reduction, eventually resulting in tiny genomes where only those genes essential to immediate survival and those beneficial to the host remain. In the marine environment, invertebrates such as tunicates are known to harbor complex microbiomes implicated in the production of natural products that are toxic and probably serve a defensive function. Here, we show that the intracellular symbiont Candidatus Endolissoclinum faulkneri is a long-standing symbiont of the tunicate Lissoclinum patella, that has persisted through cryptic speciation of the host. In contrast to the known examples of insect symbionts, which tend to be either relatively recent or ancient relationships, the genome of Ca. E. faulkneri has a very low coding density but very few recognizable pseudogenes. The almost complete degradation of intergenic regions and stable gene inventory of extant strains of Ca. E. faulkneri show that further degradation and deletion is happening very slowly. This is a novel stage of genome reduction and provides insight into how tiny genomes are formed. The ptz pathway, which produces the defensive patellazoles, is shown to date to before the divergence of Ca. E. faulkneri strains, reinforcing its importance in this symbiotic relationship. Lastly, as in insects we show that stable symbionts can be lost, as we describe an L. patella animal where Ca. E. faulkneri is displaced by a likely intracellular pathogen. Our results suggest that intracellular symbionts may be an important source of ecologically significant natural products in animals.

SUBMITTER: Kwan JC

PROVIDER: S-EPMC3851785 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Bacterial endosymbiosis in a chordate host: long-term co-evolution and conservation of secondary metabolism.

Kwan Jason C JC Schmidt Eric W EW

PloS one 20131204 12

Intracellular symbiosis is known to be widespread in insects, but there are few described examples in other types of host. These symbionts carry out useful activities such as synthesizing nutrients and conferring resistance against adverse events such as parasitism. Such symbionts persist through host speciation events, being passed down through vertical transmission. Due to various evolutionary forces, symbionts go through a process of genome reduction, eventually resulting in tiny genomes wher ...[more]

PMID: 24324632

Similar Datasets

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.

Dataset Information

Bacterial endosymbiosis in a chordate host: long-term co-evolution and conservation of secondary metabolism.

Publications

Bacterial endosymbiosis in a chordate host: long-term co-evolution and conservation of secondary metabolism.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets