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Obligate insect endosymbionts exhibit increased ortholog length variation and loss of large accessory proteins concurrent with genome shrinkage.

Kenyon LJ, Sabree ZL - Genome Biol Evol (2014)

Bottom Line: Upon examination of protein, functional domain, and nondomain region lengths, we found that proteins were not uniformly shrinking with genome reduction, but instead increased length variability and variability was observed in both the functional domain and nondomain regions.Additionally, as complete gene loss also contributes to overall genome shrinkage, we found that the largest proteins in the proteomes of nonhost-restricted bacteroidetial and gammaproteobacterial species often were inferred to be involved in secondary metabolic processes, extracellular sensing, or of unknown function.Therefore, loss of genes encoding large proteins not required for host-restricted lifestyles in obligate endosymbiont proteomes likely contributes to extreme genome reduction to a greater degree than gene shrinkage.

View Article: PubMed Central - PubMed

Affiliation: Department of Evolution, Ecology and Organismal Biology, The Ohio State University.

ABSTRACT
Extreme genome reduction has been observed in obligate intracellular insect mutualists and is an assumed consequence of fixed, long-term host isolation. Rapid accumulation of mutations and pseudogenization of genes no longer vital for an intracellular lifestyle, followed by deletion of many genes, are factors that lead to genome reduction. Size reductions in individual genes due to small-scale deletions have also been implicated in contributing to overall genome shrinkage. Conserved protein functional domains are expected to exhibit low tolerance for mutations and therefore remain relatively unchanged throughout protein length reduction while nondomain regions, presumably under less selective pressures, would shorten. This hypothesis was tested using orthologous protein sets from the Flavobacteriaceae (phylum: Bacteroidetes) and Enterobacteriaceae (subphylum: Gammaproteobacteria) families, each of which includes some of the smallest known genomes. Upon examination of protein, functional domain, and nondomain region lengths, we found that proteins were not uniformly shrinking with genome reduction, but instead increased length variability and variability was observed in both the functional domain and nondomain regions. Additionally, as complete gene loss also contributes to overall genome shrinkage, we found that the largest proteins in the proteomes of nonhost-restricted bacteroidetial and gammaproteobacterial species often were inferred to be involved in secondary metabolic processes, extracellular sensing, or of unknown function. These proteins were absent in the proteomes of obligate insect endosymbionts. Therefore, loss of genes encoding large proteins not required for host-restricted lifestyles in obligate endosymbiont proteomes likely contributes to extreme genome reduction to a greater degree than gene shrinkage.

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Enterobacteriaceae (a) and Flavobacteriaceae (b) average orthologous domain lengths as a function of genome size. The variance for the OIE data points is 0.63 and 2.29 for Enterobacteriaceae and Flavobacteriaceae, respectively. For the nonOIE it is 0.26 and 0.87, respectively. Y-axis values are the average ortholog lengths in number of amino acid residues.
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evu055-F2: Enterobacteriaceae (a) and Flavobacteriaceae (b) average orthologous domain lengths as a function of genome size. The variance for the OIE data points is 0.63 and 2.29 for Enterobacteriaceae and Flavobacteriaceae, respectively. For the nonOIE it is 0.26 and 0.87, respectively. Y-axis values are the average ortholog lengths in number of amino acid residues.

Mentions: If functional domains are under greater selection than linker regions due to their role in enzyme activity, then, as genome sizes decrease, average protein lengths were expected to decrease while average functional domain lengths remained fixed. However, average orthologous domain lengths were positively correlated (P < 0.05) with genome size in both families (fig. 2a and b), and the variance of average OIE domain lengths was greater than nonOIE average domain lengths. Both bacterial lineages exhibited significant positive correlations between the average total protein lengths and the average domain lengths (fig. 3a and c). Additionally, several domains showed significantly (t-test P < 0.05) greater lengths in the OIE proteins than in the nonOIE proteins. Therefore, domain lengths did not remain fixed as genome length varied in either lineage (fig. 2a and b). Instead, these data show that domain lengths in OIE proteins are more variable than in nonOIE orthologs.Fig. 2.—


Obligate insect endosymbionts exhibit increased ortholog length variation and loss of large accessory proteins concurrent with genome shrinkage.

Kenyon LJ, Sabree ZL - Genome Biol Evol (2014)

Enterobacteriaceae (a) and Flavobacteriaceae (b) average orthologous domain lengths as a function of genome size. The variance for the OIE data points is 0.63 and 2.29 for Enterobacteriaceae and Flavobacteriaceae, respectively. For the nonOIE it is 0.26 and 0.87, respectively. Y-axis values are the average ortholog lengths in number of amino acid residues.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4007534&req=5

evu055-F2: Enterobacteriaceae (a) and Flavobacteriaceae (b) average orthologous domain lengths as a function of genome size. The variance for the OIE data points is 0.63 and 2.29 for Enterobacteriaceae and Flavobacteriaceae, respectively. For the nonOIE it is 0.26 and 0.87, respectively. Y-axis values are the average ortholog lengths in number of amino acid residues.
Mentions: If functional domains are under greater selection than linker regions due to their role in enzyme activity, then, as genome sizes decrease, average protein lengths were expected to decrease while average functional domain lengths remained fixed. However, average orthologous domain lengths were positively correlated (P < 0.05) with genome size in both families (fig. 2a and b), and the variance of average OIE domain lengths was greater than nonOIE average domain lengths. Both bacterial lineages exhibited significant positive correlations between the average total protein lengths and the average domain lengths (fig. 3a and c). Additionally, several domains showed significantly (t-test P < 0.05) greater lengths in the OIE proteins than in the nonOIE proteins. Therefore, domain lengths did not remain fixed as genome length varied in either lineage (fig. 2a and b). Instead, these data show that domain lengths in OIE proteins are more variable than in nonOIE orthologs.Fig. 2.—

Bottom Line: Upon examination of protein, functional domain, and nondomain region lengths, we found that proteins were not uniformly shrinking with genome reduction, but instead increased length variability and variability was observed in both the functional domain and nondomain regions.Additionally, as complete gene loss also contributes to overall genome shrinkage, we found that the largest proteins in the proteomes of nonhost-restricted bacteroidetial and gammaproteobacterial species often were inferred to be involved in secondary metabolic processes, extracellular sensing, or of unknown function.Therefore, loss of genes encoding large proteins not required for host-restricted lifestyles in obligate endosymbiont proteomes likely contributes to extreme genome reduction to a greater degree than gene shrinkage.

View Article: PubMed Central - PubMed

Affiliation: Department of Evolution, Ecology and Organismal Biology, The Ohio State University.

ABSTRACT
Extreme genome reduction has been observed in obligate intracellular insect mutualists and is an assumed consequence of fixed, long-term host isolation. Rapid accumulation of mutations and pseudogenization of genes no longer vital for an intracellular lifestyle, followed by deletion of many genes, are factors that lead to genome reduction. Size reductions in individual genes due to small-scale deletions have also been implicated in contributing to overall genome shrinkage. Conserved protein functional domains are expected to exhibit low tolerance for mutations and therefore remain relatively unchanged throughout protein length reduction while nondomain regions, presumably under less selective pressures, would shorten. This hypothesis was tested using orthologous protein sets from the Flavobacteriaceae (phylum: Bacteroidetes) and Enterobacteriaceae (subphylum: Gammaproteobacteria) families, each of which includes some of the smallest known genomes. Upon examination of protein, functional domain, and nondomain region lengths, we found that proteins were not uniformly shrinking with genome reduction, but instead increased length variability and variability was observed in both the functional domain and nondomain regions. Additionally, as complete gene loss also contributes to overall genome shrinkage, we found that the largest proteins in the proteomes of nonhost-restricted bacteroidetial and gammaproteobacterial species often were inferred to be involved in secondary metabolic processes, extracellular sensing, or of unknown function. These proteins were absent in the proteomes of obligate insect endosymbionts. Therefore, loss of genes encoding large proteins not required for host-restricted lifestyles in obligate endosymbiont proteomes likely contributes to extreme genome reduction to a greater degree than gene shrinkage.

Show MeSH