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. 2011 Apr;21(4):599-609.
doi: 10.1101/gr.115592.110. Epub 2011 Jan 26.

Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes

Ovidiu Popa  1 , Einat Hazkani-Covo, Giddy Landan, William Martin, Tal Dagan
Affiliations

Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes

Ovidiu Popa et al. Genome Res. 2011 Apr.

Abstract

Lateral gene transfer (LGT) plays a major role in prokaryote evolution with only a few genes that are resistant to it; yet the nature and magnitude of barriers to lateral transfer are still debated. Here, we implement directed networks to investigate donor-recipient events of recent lateral gene transfer among 657 sequenced prokaryote genomes. For 2,129,548 genes investigated, we detected 446,854 recent lateral gene transfer events through nucleotide pattern analysis. Among these, donor-recipient relationships could be specified through phylogenetic reconstruction for 7% of the pairs, yielding 32,028 polarized recent gene acquisition events, which constitute the edges of our directed networks. We find that the frequency of recent LGT is linearly correlated both with genome sequence similarity and with proteome similarity of donor-recipient pairs. Genome sequence similarity accounts for 25% of the variation in gene-transfer frequency, with proteome similarity adding only 1% to the variability explained. The range of donor-recipient GC content similarity within the network is extremely narrow, with 86% of the LGTs occurring between donor-recipient pairs having ≤5% difference in GC content. Hence, genome sequence similarity and GC content similarity are strong barriers to LGT in prokaryotes. But they are not insurmountable, as we detected 1530 recent transfers between distantly related genomes. The directed network revealed that recipient genomes of distant transfers encode proteins of nonhomologous end-joining (NHEJ; a DNA repair mechanism) far more frequently than the recipient lacking that mechanism. This implicates NHEJ in genes spread across distantly related prokaryotes through bypassing the donor-recipient sequence similarity barrier.

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Figures

Figure 1.
Figure 1.
(A) A directed network. The circles represent nodes in the network. Arrows represent directed edges connecting between nodes. Edge weights are denoted by Arabic numerals attached to the edge. (B) A binary matrix representation of the directed network. If there exists a directed edge from node i to node j in the matrix, then cell aij = 1. Otherwise, aij = 0. The number of ingoing edges (IN degree) of each node is defined as the sum of the corresponding column. The number of outgoing edges (OUT degree) of each node is the sum of the corresponding row. (C) A weighted matrix representation of the directed network. Cells in the matrix correspond to the edge weight of edges connecting between nodes i and j. The column sums are the total edge weight of ingoing edges. The row sums are the total edge weight of outgoing edges.
Figure 2.
Figure 2.
(A) The directed network of recent lateral gene transfers. Node color corresponds to the taxonomic group of donors and recipients listed at the bottom. Connected components of endosymbionts are marked with numbers: (1) Helicobacter, (2) Coxiella, (3) Bartonella, (4) Leptospira, (5) Legionella, (6) Ehrlichia. Clusters of cyanobacteria are marked with letters: (a) high-light adapted Prochlorococcus, (b) low-light adapted Prochlorococcus, (c) marine Synechococcus, (d) other Synechococcus, (e) Nostocales and Chroococcales. Enlarged images of clusters (right) are marked with asterisks. Species names are written by the vertices. Annotations of transferred genes appear next to the edges. (B) Community structure within the largest connected component of the dLGT network (for the entire network, see Supplemental Fig. S2). Vertices that are grouped into the same module are colored the same. (C) Pathogens in the largest connected component of the dLGT network (for the entire network, see Supplemental Fig. S6). The arrow marks a nonpathogen (Bukholderia thailandensis) within a pathogenic community.
Figure 3.
Figure 3.
Distribution of connectivity and edge weight in the dLGT network.
Figure 4.
Figure 4.
Comparison of genome similarity measures for donor–recipient pairs and disconnected pairs.
Figure 5.
Figure 5.
Comparison of genome similarity measures between NHEJ-positive and NHEJ-negative recipients.
Figure 6.
Figure 6.
Frequency of transferred genes by functional category and donor–recipient genome similarity.
See this image and copyright information in PMC

References

    1. Altenhoff AM, Dessimoz C 2009. Phylogenetic and functional assessment of orthologs inference projects and methods. PLoS Comput Biol 5: e1000262 doi: 10.1371/journal.pcbi.1000262 - PMC - PubMed
    1. Aravind L, Koonin EV 2001. Prokaryotic homologs of the eukaryotic DNA-end-binding protein Ku, novel domains in the Ku protein and prediction of a prokaryotic double-strand break repair system. Genome Res 11: 1365–1374 - PMC - PubMed
    1. Barabási AL, Albert R, Jeong H 2000. Scale-free characteristics of random networks: the topology of the World-Wide Web. Physica A 281: 69–77
    1. Bassing CH, Alt FW 2004. The cellular response to general and programmed DNA double strand breaks. DNA Repair 3: 781–796 - PubMed
    1. Benjamini Y, Hochberg Y 1995. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57: 289–300

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