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Genome evolution in bacterial endosymbionts of insects

Key Points

  • Many insect species rely on obligate intracellular bacterial symbionts (known as primary or 'P-endosymbionts') that are generally thought to have a role in the nutrition of the host.

  • The strict maternal transmission through host lineages and lack of recombination of P-endosymbionts decreases their effective population sizes and therefore increases the effect of genetic drift in these bacterial lineages.

  • The recent full genome sequences of Buchnera, the endosymbiont that is associated with aphids, and Wigglesworthia, which lives in tsetse flies, have shed light on the process of genome reduction and on the current metabolic potential of these mutualists.

  • The dynamics of severe genome reduction in P-endosymbionts can be reconstructed by comparing endosymbiont genomes with those of their close free-living relatives. These analyses have illustrated, for example, the importance of large deletion events in the early evolution of Buchnera.

  • A comparison of two Buchnera genomes shows unprecedented genome stasis over the 50–70 million years of their evolution.

  • The many parallels between obligate mutualists and pathogens include the loss of metabolic diversity and DNA repair functions.

  • In contrast to intracellular pathogens, endosymbiont genomes retain traits that are beneficial to the host. These include amino-acid biosynthesis in Buchnera and vitamin B production in Wigglesworthia.

  • Compared with Buchnera, Wigglesworthia retains many attributes of free-living or parasitic bacteria, including a robust cell membrane and a complete flagellar apparatus.

  • Although certain bacterial mutualists use invasion strategies that are homologous to those of pathogens, the absence of these pathways in Buchnera reflects their long-term co-evolution with the host. In Wigglesworthia, the maintenance of flagellar proteins that might function in type III secretion reflects a more recent transition to endosymbiosis and/or encounters with host defences.

Abstract

Many insect species rely on intracellular bacterial symbionts for their viability and fecundity. Large-scale DNA-sequence analyses are revealing the forces that shape the evolution of these bacterial associates and the genetic basis of their specialization to an intracellular lifestyle. The full genome sequences of two obligate mutualists, Buchnera aphidicola of aphids and Wigglesworthia glossinidia of tsetse flies, reveal substantial gene loss and an integration of host and symbiont metabolic functions. Further genomic comparisons should reveal the generality of these features among bacterial mutualists and the extent to which they are shared with other intracellular bacteria, including obligate pathogens.

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Figure 1: Long-term cospeciation between P-endosymbionts and their insect hosts.
Figure 2: Phylogenetic relationships among selected symbiotic Eubacteria.
Figure 3: Comparison of genome sizes and %G+C content of selected bacterial genomes.

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Acknowledgements

The author thanks S. Aksoy, N. A. Moran and members of their labs for helpful discussions about endosymbiont genomics and for sharing insights from new data. I am also grateful to A. B. Lazarus, P. H. Degnan, R. R. Lawler, S. Aksoy and one anonymous reviewer for valuable comments on the manuscript. Any errors are the sole responsibility of the author. This work was made possible by support to J.J.W. from the National Institutes of Health, the National Science Foundation, and the Josephine Bay Paul and C. Michael Paul Foundation.

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Glossary

OBLIGATE MUTUALIST

A beneficial symbiont that lives exclusively in the host and depends on the host for survival. Obligate endosymbionts live in host cells and include diverse bacterial associates of insects.

SHOT-GUN LIBRARY

A library in which a DNA sample is broken into small pieces, cloned into vectors and sequenced. On the basis of overlap among the pieces, the various fragments can be assembled to infer the sequence of the original, intact molecules.

METABOLIC POTENTIAL

This constitutes the full range of biochemical abilities encoded by the genome of an organism, including energy and macromolecule (for example, DNA) metabolism, biosynthetic functions, degradation abilities, regulatory functions and cellular processes.

FACULTATIVE MUTUALIST

A beneficial symbiont that associates with the host, but can also live apart from it. Facultative bacterial mutualists include Vibrio fischeri of squid and Rhizobium spp. of legumes, both of which have a free-living phase to their life cycle.

COSPECIATION

The parallel evolution of two associated taxa (such as a host and a symbiont), such that speciation events in the two taxa are coupled. Congruent phylogenies of host and symbiont are highly suggestive of cospeciation, but alternative hypotheses (such as geographic factors) are also possible.

PROTEOBACTERIA

A phylum in the domain Eubacteria that includes several phylogenetic subdivisions: the alpha (α), beta (β), gamma (γ), delta (δ) and epsilon (ɛ) Proteobacteria.

ENTEROBACTERIA

(also called enteric bacteria). Gram-negative bacteria in the family Enterobacteriaceae. They are defined as being fermentative, facultatively anaerobic and oxidase-negative rods. These bacteria group with the γ-3 subdivision of Proteobacteria, and are found in the guts of humans and other animals, in soil and in water.

SECONDARY ENDOSYMBIONTS

Facultative bacterial endosymbionts of insects that are often located in syncytial cells near the bacteriocytes and in various other insect tissue types. Secondary symbionts are not essential for host survival and transfer among host individuals and species.

RANDOM GENETIC DRIFT

Changes in the frequencies of alleles or genotypes due to chance alone. Drift has a particularly important role in small populations.

EFFECTIVE POPULATION SIZE

(Ne). Formulated by Wright in 1931, Ne reflects the size of an idealized population that would experience drift in the same way as the actual (census) population. Ne can be lower than census population size due to various factors, including a history of population bottlenecks and reduced recombination.

NEARLY-NEUTRAL EVOLUTION

A model of evolution developed by T. Ohta in 1973 that emphasizes the effect of deleterious mutations with very slight fitness costs (small selective coefficients). These slightly deleterious mutations are fixed (reach a frequency of 100%) at higher rates in small populations, which are more prone to the effects of genetic drift.

TRANSOVARIAL

A mode of vertical transmission whereby the female host transmits a symbiont through her eggs to the next generation.

OVARIOLE

A functional unit of the ovary in which the eggs are produced.

MULLER'S RATCHET

The process by which the number of deleterious mutations increases irreversibly in asexual populations owing to the inability to recover the most fit class by recombination. The process is named after H. J. Muller, who described it in 1964.

LATERAL GENE TRANSFER

The transfer of genetic material from one genome to another, specifically between divergent lineages or different species. Also called horizontal gene transfer.

16S AND 23S RRNA

The 16S ribosomal RNA combines with several ribosomal proteins to form the small subunit (30S) ribosome in prokaryotes, whereas the 23S rRNA combines with 5S rRNA and proteins to form the large subunit (50S) ribosome. Heterogeneous rates of evolution among sites make these rRNA genes extremely useful for bacterial phylogenetics.

BOOTSTRAP ANALYSIS

A type of statistical analysis to test the reliability of certain branches in the evolutionary tree. The bootstrap proceeds by re-sampling the original data, with replacement, to create a series of bootstrap samples of the same size as the original data. The bootstrap value of a node is the percentage of times that a node is present in the set of trees that is constructed from the new data sets.

CODON BIAS

The non-random use of synonymous codons for a particular amino acid. In Escherichia coli, codon bias results from selection that favours the use of codons with high translational efficiency, and is much stronger at highly expressed genes. The codon adaptation index (CAI) measures the extent to which a gene uses the presumed most efficient codons.

SYNONYMOUS SUBSTITUTION

A nucleotide change in a DNA sequence that does not result in a change in the encoded amino acid.

NON-SYNONYMOUS SUBSTITUTION

A change in nucleotide sequence that alters the encoded amino acid.

CHAPERONIN

A category of protein that functions in protein folding, intercellular signalling and other activities. Chaperonins are also named 'heat-shock proteins' due to their upregulated expression in bacteria that have been subjected to stress.

SELECTION COEFFICIENT

The difference in relative fitness of the most fit genotype and that of a less fit genotype. Often conceptualized as the 'strength' of natural selection on a particular trait.

PARSIMONY

As applied to phylogenetic reconstruction, a criterion for estimating historical changes by minimizing the number of events that are required to explain the observed data.

GENOME ARCHITECTURE

The structure, content and organization of a genome, including the location and order of genes.

TYPE III SECRETION

An assemblage of 20 proteins that spans the cell membrane, transports proteins out of the cell and mediates the delivery of specific proteins that suppress defences or otherwise facilitate cell invasion.

NUCLEOTIDE EXCISION REPAIR

A DNA repair pathway that removes ultraviolet-light-induced DNA damage (such as thymidine dimers) and bulky DNA adducts by excising the oligonucleotide that contains the damaged bases. The single-stranded gap is filled in by using the intact strand as a template. Involves the activity of uvrABC, among other genes.

SOS RESPONSE

The bacterial response to DNA damage that is regulated by the LexA and RecA proteins and involves the expression of a network of >20 genes, including several DNA repair enzymes.

TRICARBOXYLIC ACID CYCLE

(TCA). A series of metabolic reactions in aerobic respiration by which pyruvate is oxidized to carbon dioxide.

UBIQUINONE Q

A coenzyme found in aerobic organisms, so named because it was thought to be universal in animal tissues.

ABC TRANSPORT SYSTEM

The largest family of membrane transport proteins that are ubiquitous across prokaryotes and eukaryotes. These proteins translocate nutrients and other substrates across the membrane, often against a concentration gradient, by hydrolysing ATP.

QUORUM SENSING

A mechanism used by many bacterial pathogens and mutualists to detect critical bacterial cell numbers in host tissues. Cell densities are indicated by the concentration on autoinducers, which regulate the expression of specific genes.

TWO-COMPONENT REGULATORY SYSTEM

A gene regulatory system that involves a sensor kinase and a response regulator. It triggers rapid changes in gene expression in response to contact with the host or to environmental changes in the host.

OUTER MEMBRANE PROTEINS

(OMP). A group of membrane proteins, including porins and certain receptors, that act in host invasion, adhesion and colonization, and show many genetic and regulatory mechanisms. These proteins are important for interacting with host defences and for the permeability of antimicrobial substances.

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Wernegreen, J. Genome evolution in bacterial endosymbionts of insects. Nat Rev Genet 3, 850–861 (2002). https://doi.org/10.1038/nrg931

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