Extreme genome reduction in symbiotic bacteria

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Abstract

Since 2006, numerous cases of bacterial symbionts with extraordinarily small genomes have been reported. These organisms represent independent lineages from diverse bacterial groups. They have diminutive gene sets that rival some mitochondria and chloroplasts in terms of gene numbers and lack genes that are considered to be essential in other bacteria. These symbionts have numerous features in common, such as extraordinarily fast protein evolution and a high abundance of chaperones. Together, these features point to highly degenerate genomes that retain only the most essential functions, often including a considerable fraction of genes that serve the hosts. These discoveries have implications for the concept of minimal genomes, the origins of cellular organelles, and studies of symbiosis and host-associated microbiota.

Key Points

  • Prior to 2006, the smallest known cellular genomes, from several bacterial and archaeal phyla, reached a lower limit of about 500 kb, or approximately 500 genes.

  • Starting with 'Candidatus Carsonella ruddii' in 2006, several much smaller genomes have recently been reported, all from bacteria that are intracellular symbionts of insects. These represent independent lineages of symbiotic bacteria in the Gammaproteobacteria, Betaproteobacteria, Alphaproteobacteria and Bacteroidetes taxa and have genome sizes of 139–250 kb, encoding a total of only 121–227 proteins.

  • In addition to extreme genome reduction, these organisms show extreme biases in genomic GC content, massive acceleration in the rates of protein evolution and unusual, degenerate cell morphologies. They also exhibit constitutively elevated expression of chaperonin and other heat shock proteins.

  • Despite their small sizes, all of these genomes retain a set of genes encoding enzymes involved in biosynthetic pathways for the production of nutrients that are needed by the insect hosts.

  • Although none of these symbionts has been grown in pure culture outside of the host, these organisms, with the exception of 'Candidatus Tremblaya princeps', retain most of the core genes for DNA replication, transcription and translation. Thus, although their genome sizes approach those of organelles (mitochondria and plastids), their gene sets are much more 'cell like' than those of organelles.

  • Thus far, no evidence supports the importation of host-encoded proteins into the cytosol of symbionts, and no evidence supports the transfer of ancestral symbiont genes to the host nucleus.

  • In the exceptional case of 'Ca. Tremblaya princeps', with a genome of only 139 kb, the cell machinery has undergone a radical depletion; for example, all tRNA synthetases are absent, in striking contrast to the other tiny genomes described to date. This gene loss may reflect a dependence on the highly unusual presence of a second bacterial symbiont living within 'Ca. Tremblaya princeps'.

  • These symbionts with tiny genomes give insight into the nature of essential genes and the limits of cell and genome evolution.

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Figure 1: Comparison of the smallest genomes for free-living and symbiotic organisms.
Figure 2: Extreme genomic features in symbionts with tiny genomes.
Figure 3: Stages of genome reduction in host-restricted bacteria for which small population sizes and an asexual life cycle result in mutation fixation.

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Acknowledgements

Part of the work leading to this Review was supported by US National Science Foundation (NSF) awards 0626716 and 1062363 to N.A.M., and J.P.M. was supported by the NSF Montana Experimental Program to Stimulate Competitive Research grant EPS-0701906 during the writing of this Review.

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Axenic culture

A culture of a bacterium or other organism that is independent of any other living organism.

Endosymbionts

Symbionts that reside inside the cells of the host.

Bacteriocytes

Specialized eukaryotic cells that contain symbionts within the cytosol.

Psyllid

A type of small insect that feeds on plant phloem sap.

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