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. 2016 Jan 8;11(1):2.
doi: 10.1186/s13062-015-0104-3.

The mysterious orphans of Mycoplasmataceae

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The mysterious orphans of Mycoplasmataceae

Tatiana V Tatarinova et al. Biol Direct. .

Abstract

Background: The length of a protein sequence is largely determined by its function. In certain species, it may be also affected by additional factors, such as growth temperature or acidity. In 2002, it was shown that in the bacterium Escherichia coli and in the archaeon Archaeoglobus fulgidus, protein sequences with no homologs were, on average, shorter than those with homologs (BMC Evol Biol 2:20, 2002). It is now generally accepted that in bacterial and archaeal genomes the distributions of protein length are different between sequences with and without homologs. In this study, we examine this postulate by conducting a comprehensive analysis of all annotated prokaryotic genomes and by focusing on certain exceptions.

Results: We compared the distribution of lengths of "having homologs proteins" (HHPs) and "non-having homologs proteins" (orphans or ORFans) in all currently completely sequenced and COG-annotated prokaryotic genomes. As expected, the HHPs and ORFans have strikingly different length distributions in almost all genomes. As previously established, the HHPs, indeed are, on average, longer than the ORFans, and the length distributions for the ORFans have a relatively narrow peak, in contrast to the HHPs, whose lengths spread over a wider range of values. However, about thirty genomes do not obey these rules. Practically all genomes of Mycoplasma and Ureaplasma have atypical ORFans distributions, with the mean lengths of ORFan larger than the mean lengths of HHPs. These genera constitute over 80 % of atypical genomes.

Conclusions: We confirmed on a ubiquitous set of genomes that the previous observation of HHPs and ORFans have different gene length distributions. We also showed that Mycoplasmataceae genomes have very distinctive distributions of ORFans lengths. We offer several possible biological explanations of this phenomenon, such as an adaptation to Mycoplasmataceae's ecological niche, specifically its "quiet" co-existence with host organisms, resulting in long ABC transporters.

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Figures

Fig. 1
Fig. 1
Histograms of protein lengths of Coxiella burnetii (a), Mycobacterium leprae (b), Chlamydia trachomatis (c), Rickettsia prowazekii (d) and all other prokaryotes (e) and (f) tested in this study. The X axis corresponds to the protein length intervals (0 -- (0100], 100-- (100,200], etc.), while the Y axis show the relative frequency of ORFans and HHPs among the genomes. Bar plot and the relative frequency plot with a smaller bin size for all prokaryotes are presented on Panels (e) and (f), respectively
Fig. 2
Fig. 2
The difference between mean lengths of HHPs and ORFans for 1484 prokaryotic genomes. The X axis corresponds to the difference between mean length of HHPs and ORFans, and the Y axis shows the relative frequency of genomes with the given length difference. For all prokaryotic genomes, HHPs are longer than ORFans by, on average, 144 amino acids. For the Mycoplasmataceae genomes, the average difference is only 14 amino acids, while 17 out of 37 Mycoplasmataceae genomes have ORFans that are, on average, longer than HHPs
Fig. 3
Fig. 3
Mean (a) and Median (b) ORFans’ length vs. average HHP length for selected eight groups of prokaryotes. Each point represents a genome. Family Mycoplasmataceae (pink), family Mycobacteriaceae (red), genus Agrobacterium (blue), genus Bacillus (green), genus Anaplasma (orange), genus Ehrlichia (dark green), genus Neorickettsia (black) and genus Campylobacter (grey) are shown. The regression line shows the relationships between the mean HHP length and the mean ORFan length across 1484 annotated prokaryotic genomes
Fig. 4
Fig. 4
Histograms of protein lengths of (a) M. genitalium (M. genitalium G37 uid57707, NC_000908) and (b) M. hyopneumonia (M. hyopneumoniae 232 uid58205, NC_006360) X axis labels correspond to the following protein length intervals 0 -- (0100], 100-- (100,200], etc. Y axis shows a relative frequency of the protein with a given length in a genome
Fig. 5
Fig. 5
Genomic GC content (Panel a) and genic GC3 content (Panel b) in annotated species of Mycoplasmataceae. Grey histograms correspond to all prokaryotes while red histograms correspond to selected Mycoplasma species. Horizontal axis shows GC (a) and GC3 content, and vertical axis shows the number of prokaryotic genomes with the given content

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