Dataset Information

On the origin of microbial ORFans: quantifying the strength of the evidence for viral lateral transfer.

ABSTRACT:

Background

The origin of microbial ORFans, ORFs having no detectable homology to other ORFs in the databases, is one of the unexplained puzzles of the post-genomic era. Several hypothesis on the origin of ORFans have been suggested in the last few years, most of which based on selected, relatively small, subsets of ORFans. One of the hypotheses for the origin of ORFans is that they have been acquired thru lateral transfer from viruses. Here we carry out a comprehensive, genome-wide study on the origins of ORFans to quantify the strength of current evidence supporting this hypothesis.

Results

We performed similarity searches by querying all current ORFans against the public virus protein database. Surprisingly, we found that only 2.8% of all microbial ORFans have detectable homologs in viruses, while the percentage of non-ORFans with detectable homologs in viruses is 7.9%, a significantly higher figure. This suggests that the current evidence for the origin of ORFans from lateral transfer from viruses is at best weak. However, an analysis of individual genomes revealed a number of organisms with much higher percentages, many of them belonging to the Firmicutes and Gamma-proteobacteria. We provide evidence suggesting that the current virus database may be biased towards those viruses attacking Firmicutes and Gamma-proteobacteria.

Conclusion

We conclude that as more viral genomes are sequenced, more microbial ORFans will find homologs in viruses, but this trend may vary much for individual genomes. Thus, lateral transfer from viruses alone is unlikely to explain the origin of the majority of ORFans in the majority of prokaryotes and consequently, other, not necessarily exclusive, mechanisms are likely to better explain the origin of the increasing number of ORFans.

SUBMITTER: Yin Y

PROVIDER: S-EPMC1559721 | biostudies-literature | 2006 Aug

REPOSITORIES: biostudies-literature

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Publications

On the origin of microbial ORFans: quantifying the strength of the evidence for viral lateral transfer.

Yin Yanbin Y Yin Yanbin Y Fischer Daniel D

BMC evolutionary biology 20060816

<h4>Background</h4>The origin of microbial ORFans, ORFs having no detectable homology to other ORFs in the databases, is one of the unexplained puzzles of the post-genomic era. Several hypothesis on the origin of ORFans have been suggested in the last few years, most of which based on selected, relatively small, subsets of ORFans. One of the hypotheses for the origin of ORFans is that they have been acquired thru lateral transfer from viruses. Here we carry out a comprehensive, genome-wide study ...[more]

PMID: 16914045

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Project description:BackgroundGenome-wide studies have already shed light into the evolution and enormous diversity of the viral world. Nevertheless, one of the unresolved mysteries in comparative genomics today is the abundance of ORFans - ORFs with no detectable sequence similarity to any other ORF in the databases. Recently, studies attempting to understand the origin and functions of bacterial ORFans have been reported. Here we present a first genome-wide identification and analysis of ORFans in the viral world, with focus on bacteriophages.ResultsAlmost one-third of all ORFs in 1,456 complete virus genomes correspond to ORFans, a figure significantly larger than that observed in prokaryotes. Like prokaryotic ORFans, viral ORFans are shorter and have a lower GC content than non-ORFans. Nevertheless, a statistically significant lower GC content is found only on a minority of viruses. By focusing on phages, we find that 38.4% of phage ORFs have no homologs in other phages, and 30.1% have no homologs neither in the viral nor in the prokaryotic world. Phages with different host ranges have different percentages of ORFans, reflecting different sampling status and suggesting various diversities. Similarity searches of the phage ORFeome (ORFans and non-ORFans) against prokaryotic genomes shows that almost half of the phage ORFs have prokaryotic homologs, suggesting the major role that horizontal transfer plays in bacterial evolution. Surprisingly, the percentage of phage ORFans with prokaryotic homologs is only 18.7%. This suggests that phage ORFans play a lesser role in horizontal transfer to prokaryotes, but may be among the major players contributing to the vast phage diversity.ConclusionAlthough the current sampling of viral genomes is extremely low, ORFans and near-ORFans are likely to continue to grow in number as more genomes are sequenced. The abundance of phage ORFans may be partially due to the expected vast viral diversity, and may be instrumental in understanding viral evolution. The functions, origins and fates of the majority of viral ORFans remain a mystery. Further computational and experimental studies are likely to shed light on the mechanisms that have given rise to so many bacterial and viral ORFans.

Project description:UNLABELLED:Unraveling the drivers controlling the response and adaptation of biological communities to environmental change, especially anthropogenic activities, is a central but poorly understood issue in ecology and evolution. Comparative genomics studies suggest that lateral gene transfer (LGT) is a major force driving microbial genome evolution, but its role in the evolution of microbial communities remains elusive. To delineate the importance of LGT in mediating the response of a groundwater microbial community to heavy metal contamination, representative Rhodanobacter reference genomes were sequenced and compared to shotgun metagenome sequences. 16S rRNA gene-based amplicon sequence analysis indicated that Rhodanobacter populations were highly abundant in contaminated wells with low pHs and high levels of nitrate and heavy metals but remained rare in the uncontaminated wells. Sequence comparisons revealed that multiple geochemically important genes, including genes encoding Fe(2+)/Pb(2+) permeases, most denitrification enzymes, and cytochrome c553, were native to Rhodanobacter and not subjected to LGT. In contrast, the Rhodanobacter pangenome contained a recombinational hot spot in which numerous metal resistance genes were subjected to LGT and/or duplication. In particular, Co(2+)/Zn(2+)/Cd(2+) efflux and mercuric resistance operon genes appeared to be highly mobile within Rhodanobacter populations. Evidence of multiple duplications of a mercuric resistance operon common to most Rhodanobacter strains was also observed. Collectively, our analyses indicated the importance of LGT during the evolution of groundwater microbial communities in response to heavy metal contamination, and a conceptual model was developed to display such adaptive evolutionary processes for explaining the extreme dominance of Rhodanobacter populations in the contaminated groundwater microbiome. IMPORTANCE:Lateral gene transfer (LGT), along with positive selection and gene duplication, are the three main mechanisms that drive adaptive evolution of microbial genomes and communities, but their relative importance is unclear. Some recent studies suggested that LGT is a major adaptive mechanism for microbial populations in response to changing environments, and hence, it could also be critical in shaping microbial community structure. However, direct evidence of LGT and its rates in extant natural microbial communities in response to changing environments is still lacking. Our results presented in this study provide explicit evidence that LGT played a crucial role in driving the evolution of a groundwater microbial community in response to extreme heavy metal contamination. It appears that acquisition of genes critical for survival, growth, and reproduction via LGT is the most rapid and effective way to enable microorganisms and associated microbial communities to quickly adapt to abrupt harsh environmental stresses.

Dataset Information

On the origin of microbial ORFans: quantifying the strength of the evidence for viral lateral transfer.

Background

Results

Conclusion

Publications

On the origin of microbial ORFans: quantifying the strength of the evidence for viral lateral transfer.

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