Trends in Genetics
Volume 26, Issue 1, January 2010, Pages 5-8
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Genome Analysis
Acquisition of prokaryotic genes by fungal genomes

https://doi.org/10.1016/j.tig.2009.11.007Get rights and content

The relevance of horizontal gene transfer (HGT) in eukaryotes is a matter of debate. Recent analyses have shown clear examples in some species such as Candida parapsilosis, but broader surveys are lacking. To assess the impact of HGT in the fungal kingdom, we searched for prokaryotic-derived HGTs in 60 fully sequenced genomes. Using strict phylogenomic criteria, we detected 713 transferred genes. HGT affected most fungal clades, with particularly high rates in Pezizomycotina. Transferred genes included bacterial arsenite reductase, catalase, different racemases and peptidoglycan metabolism enzymes. Our results suggest an important role for HGT in fungal evolution.

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HGT in eukaryotes

HGT, the exchange of genetic material between two species [1], was discovered 50 years ago [2], but it is the current wealth of genomic sequences that is revealing its real impact. Currently, it is widely accepted that HGT is one of the main evolutionary driving forces in prokaryotes, but its relevance for eukaryotes remains controversial 3, 4, 5. The traditional view that HGT in eukaryotes is virtually absent has been recently challenged by genome-wide analyses reporting the transfer of

Detection of inter-domain HGT events in fungi

Using 60 complete fungal genomes and >600 other genomes from prokaryotes and other eukaryotes, we designed a phylogenomic pipeline to detect cases of genes likely to have been acquired through HGT from prokaryotic donors (see the online supplementary material). In brief, we adopted a conservative strategy that searched for genes present in few (<10) fungi and absent in other eukaryotes, but which could be found in a relatively high number of prokaryotic genomes (>30). This procedure detected

Differential impact of HGT across the fungal tree of life

We mapped the 235 HGT events on the fungal tree of life [10], assuming the transfers affected the last common ancestor of all species in a monophyletic group. Our results (Figure 1) show that HGT affected most fungal lineages to various extents. Unexpectedly, nearly two-thirds (65%) of the events are mapped within Pezizomycotina, of which one-third appear at the base of this clade. More recent HGT events affect most Pezizomycotina lineages, suggesting this is an ongoing process. By contrast,

Restoration of the arsenate detoxification pathway

We identified two independent acquisitions of a bacterial arsenate reductase in Yarrowia lipolytica and Rizopus oryzae. The reduction of arsenate to arsenite is an important step in arsenic detoxification [17], a pathway that is carried out in the yeast Saccharomyces cerevisiae by a different arsenate reductase (ARR2) in combination with membrane pumps that expel arsenite from the cytoplasm. Orthology assessment 10, 18 shows that Y. lipolytica, R. oryzae and their close relatives have no

Acquisition of multiple racemase genes

Racemases catalyze the inter-conversion of optical isomers (e.g. D- and L-amino acids). Recent studies describe putative cases of HGT involving various bacterial racemases in eukaryotic genomes. These include alanine racemase in Schizosaccharomyces pombe[11] and Adineta vaga[7], and a proline racemase in C. parapsilosis[15]. Interestingly, our survey detected seven additional HGT instances involving three different racemases: aspartate, hydantoin and mandelate racemases. Most such cases involve

Bacterial catalases in fungal pathogenic species

Through their action in decomposing reactive oxygen species, catalases can help pathogens overcome host defense mechanisms. The potential advantages conferred by the acquisition of foreign catalases have been extensively studied in pathogenic bacteria 21, 22. In fungi, a recent transfer of a bacterial catalase has been described in the microsporidian pathogen Nosema locustae[23]. In our study, we detected similar transfers to three important plant pathogens: the Dothideomycetes Stagonospora

Transfer of a Mur operon

Multiple transfers of functionally-related enzymes are remarkable because they can provide the recipient species with a novel metabolic pathway. Our analyses found, in similar sets of Aspergillus species, the first three enzymes of the bacterial peptidoglycan biosynthesis pathway: MurA, MurB and MurC. Recipient species included Aspergillus terreus, Aspergillus oryzae, Aspergillus flavus, Aspergillus fumigatus and Neosartorya fischeri, although MurC was apparently lost in the latter two species.

Concluding remarks

Our results reveal that inter-domain HGT is widespread in fungi and has played a role in the evolution of this eukaryotic group. We detected 713 transferred genes that, given the high stringency of our phylogenomic criteria, should be considered a minimal estimate. Additional studies will probably reveal further examples of transfers that have escaped our strict criteria (e.g. prokaryotic genes transferred to other eukaryotic groups). The ability of fungi to acquire alien prokaryotic genes

Acknowledgements

MMH and TG are supported by the FUNPATH grant from the ERA-NET pathogenomics network funded by the Spanish Ministry of Science (GEN06-27784).

References (25)

  • M. Syvanen

    Cross-species gene transfer: implications for a new theory of evolution

    J. Theor. Biol.

    (1985)
  • B.P. Rosen

    Families of arsenic transporters

    Trends Microbiol.

    (1999)
  • D.M. Faguy et al.

    Horizontal transfer of catalase-peroxidase genes between archaea and pathogenic bacteria

    Trends Genet.

    (2000)
  • T. Akiba

    On the mechanism of the development of multiple drug-resistant clones of Shigella

    Jpn. J. Microbiol.

    (1960)
  • C.G. Kurland

    What tangled web: barriers to rampant horizontal gene transfer

    Bioessays

    (2005)
  • J.O. Andersson

    Lateral gene transfer in eukaryotes

    Cell Mol. Life Sci.

    (2005)
  • P.J. Keeling et al.

    Horizontal gene transfer in eukaryotic evolution

    Nat. Rev. Genet.

    (2008)
  • G. Ricard

    Horizontal gene transfer from bacteria to rumen ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment

    BMC Genomics

    (2006)
  • E.A. Gladyshev

    Massive horizontal gene transfer in bdelloid rotifers

    Science

    (2008)
  • S. Garcia-Vallve

    Horizontal gene transfer of glycosyl hydrolases of the rumen fungi

    Mol. Biol. Evol.

    (2000)
  • J.E. Galagan

    Genomics of the fungal kingdom: insights into eukaryotic biology

    Genome Res.

    (2005)
  • M. Marcet-Houben et al.

    The tree versus the forest: the fungal tree of life and the topological diversity within the yeast phylome

    PLoS ONE

    (2009)
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