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Learning how to live together: genomic insights into prokaryote–animal symbioses

Key Points

  • The relevance of symbiotic microbial associations for evolution remained unclear for several decades for theoretical, conceptual, experimental and technological reasons. However, as Darwin emphasized, the struggle for existence includes the dependence of one organism on another.

  • The phylogenetic distribution of symbioses between eukaryotic hosts and prokaryotes is much wider than previously thought, which reinforces the view that this phenomenon has a role in promoting evolutionary innovation. The complete genome sequences for the species that are involved, and the development of metagenomic approaches, provide new opportunities for research into symbioses.

  • Numerous studies indicate that extant endosymbionts originated from ancient pathogenic bacteria that attenuated — or even domesticated — their virulence factors. Adaptation to intracellular life has also involved dramatic genomic and metabolic changes, the most remarkable being genome reduction by gene loss.

  • In many cases, hosts with primary endosymbionts are invaded by new symbionts that, although they are facultative, can provide benefits to the host. These new bacteria could take over the symbiotic functions of the initial symbiont, and so the situation might end in the replacement of one symbiont by the other. Alternatively, a microbial consortium can be established, owing to metabolic complementation between symbionts.

  • The host must also develop mechanisms to adapt its innate immune system, to house the bacteria and to control their proliferation. This is an emerging research area, and its findings provide insights into the non-pathogenicity of endosymbionts. The genome sequencing of selected hosts will be crucial for a complete overview of these associations.

  • The existence of minimal natural genomes has provided important insights for researchers who are interested in experimental genome minimization. Analyses of minimal genomes provide an estimate of the smallest number of genetic elements that are sufficient to build a modern-type free-living cellular organism — a preliminary step in the attempts to make a living cell.

Abstract

Our understanding of prokaryote–eukaryote symbioses as a source of evolutionary innovation has been rapidly increased by the advent of genomics, which has made possible the biological study of uncultivable endosymbionts. Genomics is allowing the dissection of the evolutionary process that starts with host invasion then progresses from facultative to obligate symbiosis and ends with replacement by, or coexistence with, new symbionts. Moreover, genomics has provided important clues on the mechanisms driving the genome-reduction process, the functions that are retained by the endosymbionts, the role of the host, and the factors that might determine whether the association will become parasitic or mutualistic.

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Figure 1: Comparative biochemistry of symbiont–host interdependence.
Figure 2: Bacteriocytes of the aphid Cinara cedri.
Figure 3: The flagellum, an example of genome reduction at the structural level.

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Acknowledgements

Financial support was provided by grants GV/2007/050 from Generalitat Valenciana, Spain, to R.G and BFU2006-06003 from Ministerio de Educación y Ciencia (MEC), Spain, to A.L. R.G is a recipient of a contract in the 'Ramón y Cajal' programme from the MEC, Spain. Our thanks to H. Escrivá (CNRS, Banyuls sur Mer), P. López (CNRS, Orsay) and D. Moreira (CNRS, Orsay) for their advice in the design of the eukaryotic phylogenetic tree in BOX 1.

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DATABASES

Entrez Genome Project

Acyrthosiphon pisum

Baumannia cicadellinicola

Blochmannia floridanus

Brugia malayi

Buchnera aphidicola

Caenorhabditis elegans

Carsonella ruddii

Chromobacterium violaceum

Drosophila melanogaster

Sodalis glossinidius

Sulcia muelleri

Wigglesworthia glossinidia

Wolbachia pipientis

FURTHER INFORMATION

Andrés Moya's homepage

Juli Peretó's homepage

Rosario Gil's homepage

Amparo Latorre's homepage

Cavanilles Institute web page

Genomes OnLine Database

Microbial Genome Database for Comparative Analysis

The Sanger Institute Glossina Genome Project

Glossary

Symbiosis

From the Greek, sym 'with' and biosis 'living'. A long-term association between two or more organisms of different species that is integrated at the behavioural, metabolic or genetic level. According to the level of dependence on the host, symbiosis can be obligate or facultative. The term was introduced by Anton de Bary and Albert Bernard Frank when discussing lichens and mycorrhizae, respectively, at the end of the 1870s.

Parasitism

Symbioses in which one species is increasing its fitness while the fitness of the other species is adversely affected.

Mutualism

Symbioses in which both species increase their fitness.

Commensalism

Symbioses in which one partner is increasing its fitness without affecting the other species.

Ectosymbiosis

A symbiosis in which the symbiont lives on the body surface of the host, including internal surfaces such as the lining of the digestive tube and the ducts of glands.

Endosymbiosis

Symbioses in which a prokaryote symbiont lives inside a eukaryotic cell.

Primary endosymbiont

(P-endosymbiont). Obligate bacterial endosymbionts that live inside specialized animal host cells called bacteriocytes. The association is obligate for both partners.

Secondary symbiont

(S-symbiont). Facultative bacterial endosymbiont that coexists with a P-endosymbiont. Often located in syncitial cells near the bacteriocyte and in various other insect tissue types. Secondary symbionts are not essential for host survival and are transferred horizontally among individuals of both the host species and other species.

Metagenomics

The application of genomic analyses to uncultured microorganisms. Also referred to as environmental genomics.

Vertical transmission

The endosymbionts are maternally transferred, that is, directly from a host to its offspring.

Bacteriocytes

Specialized cells of the host species in which symbiotic bacteria live.

Heterotrophy

The metabolic mode in which the carbon source is organic matter. By extension, this is a metabolic mode in which organic matter is the source of carbon, electrons and energy (chemoorganoheterotrophy).

Chemolithoautotrophy

The metabolic mode in which CO2 is the carbon source and an inorganic chemical reaction is both the electron and energy source.

Horizontal transmission

Some endosymbionts retain a generalized ability to colonize and persist in multiple hosts, that is, their transmission is between individuals of the same or different host species, rather than from parent to offspring.

Syntrophy

Emergence of new metabolic capabilities as a result of symbiosis, it is often essential for the survival of the consortium.

Bacteriome

An organ-like structure formed by bacteriocytes.

Pathogenic island

A part of a genome, for which there is evidence of its acquisition by horizontal transfer, that encodes genes that contribute to the virulence of a pathogen.

Minimal genome

The smallest set of genes that is necessary and sufficient to sustain a living cell in the most favourable conditions; that is, in the presence of adequate nutrients and in the absence of stress factors.

Synthetic biology

The design and fabrication of artificial biological systems, with the aim of either optimizing their performance in the context of their technological utility or of deepening our understanding of the naturally occurring organisms.

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Moya, A., Peretó, J., Gil, R. et al. Learning how to live together: genomic insights into prokaryote–animal symbioses. Nat Rev Genet 9, 218–229 (2008). https://doi.org/10.1038/nrg2319

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