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Multiple recent horizontal transfers of a large genomic region in cheese making fungi.

ABSTRACT: While the extent and impact of horizontal transfers in prokaryotes are widely acknowledged, their importance to the eukaryotic kingdom is unclear and thought by many to be anecdotal. Here we report multiple recent transfers of a huge genomic island between Penicillium spp. found in the food environment. Sequencing of the two leading filamentous fungi used in cheese making, P. roqueforti and P. camemberti, and comparison with the penicillin producer P. rubens reveals a 575?kb long genomic island in P. roqueforti--called Wallaby--present as identical fragments at non-homologous loci in P. camemberti and P. rubens. Wallaby is detected in Penicillium collections exclusively in strains from food environments. Wallaby encompasses about 250 predicted genes, some of which are probably involved in competition with microorganisms. The occurrence of multiple recent eukaryotic transfers in the food environment provides strong evidence for the importance of this understudied and probably underestimated phenomenon in eukaryotes.

SUBMITTER: Cheeseman K

PROVIDER: S-EPMC3896755 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Multiple recent horizontal transfers of a large genomic region in cheese making fungi.

Cheeseman Kevin K Ropars Jeanne J Renault Pierre P Dupont Joëlle J Gouzy Jérôme J Branca Antoine A Abraham Anne-Laure AL Ceppi Maurizio M Conseiller Emmanuel E Debuchy Robert R Malagnac Fabienne F Goarin Anne A Silar Philippe P Lacoste Sandrine S Sallet Erika E Bensimon Aaron A Giraud Tatiana T Brygoo Yves Y

Nature communications 20140101

While the extent and impact of horizontal transfers in prokaryotes are widely acknowledged, their importance to the eukaryotic kingdom is unclear and thought by many to be anecdotal. Here we report multiple recent transfers of a huge genomic island between Penicillium spp. found in the food environment. Sequencing of the two leading filamentous fungi used in cheese making, P. roqueforti and P. camemberti, and comparison with the penicillin producer P. rubens reveals a 575 kb long genomic island ...[more]

PMID: 24407037

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Project description:BackgroundThe most frequent case of horizontal transfer in plants involves a group I intron in the mitochondrial gene cox1, which has been acquired via some 80 separate plant-to-plant transfer events among 833 diverse angiosperms examined. This homing intron encodes an endonuclease thought to promote the intron's promiscuous behavior. A promising experimental approach to study endonuclease activity and intron transmission involves somatic cell hybridization, which in plants leads to mitochondrial fusion and genome recombination. However, the cox1 intron has not yet been found in the ideal group for plant somatic genetics - the Solanaceae. We therefore undertook an extensive survey of this family to find members with the intron and to learn more about the evolutionary history of this exceptionally mobile genetic element.ResultsAlthough 409 of the 426 species of Solanaceae examined lack the cox1 intron, it is uniformly present in three phylogenetically disjunct clades. Despite strong overall incongruence of cox1 intron phylogeny with angiosperm phylogeny, two of these clades possess nearly identical intron sequences and are monophyletic in intron phylogeny. These two clades, and possibly the third also, contain a co-conversion tract (CCT) downstream of the intron that is extended relative to all previously recognized CCTs in angiosperm cox1. Re-examination of all published cox1 genes uncovered additional cases of extended co-conversion and identified a rare case of putative intron loss, accompanied by full retention of the CCT.ConclusionsWe infer that the cox1 intron was separately and recently acquired by at least three different lineages of Solanaceae. The striking identity of the intron and CCT from two of these lineages suggests that one of these three intron captures may have occurred by a within-family transfer event. This is consistent with previous evidence that horizontal transfer in plants is biased towards phylogenetically local events. The discovery of extended co-conversion suggests that other cox1 conversions may be longer than realized but obscured by the exceptional conservation of plant mitochondrial sequences. Our findings provide further support for the rampant-transfer model of cox1 intron evolution and recommend the Solanaceae as a model system for the experimental analysis of cox1 intron transfer in plants.

Project description:Transposable elements (TEs) are dynamic elements present in all eukaryotic genomes. They can "jump" and amplify within the genome and promote segmental genome rearrangements on both autosomes and sex chromosomes by disruption of gene structures. The Bovine-B long interspersed nuclear element (Bov-B LINE) is among the most abundant TE-retrotransposon families in vertebrates due to horizontal transfer (HT) among vertebrate lineages. Recent studies have shown multiple HTs or the presence of diverse Bov-B LINE groups in the snake lineage. It is hypothesized that Bov-B LINEs are highly dynamic and that the diversity reflects multiple HTs in snake lineages. Partial sequences of Bov-B LINE from 23 snake species were characterized. Phylogenetic analysis resolved at least two Bov-B LINE groups that might correspond to henophidian and caenophidian snakes; however, the tree topology differed from that based on functional nuclear and mitochondrial gene sequences. Several Bov-B LINEs of snakes showed greater than 80% similarity to sequences obtained from insects, whereas the two Bov-B LINE groups as well as sequences from the same snake species classified in different Bov-B LINE groups showed sequence similarities of less than 80%. Calculation of estimated divergence time and pairwise divergence between all individual Bov-B LINE copies suggest invasion times ranging from 79.19 to 98.8 million years ago in snakes. Accumulation of elements in a lineage-specific fashion ranged from 9 × 10-6% to 5.63 × 10-2% per genome. The genomic proportion of Bov-B LINEs varied among snake species but was not directly associated with genome size or invasion time. No differentiation in Bov-B LINE copy number between males and females was observed in any of the snake species examined. Incongruence in tree topology between Bov-B LINEs and other snake phylogenies may reflect past HT events. Sequence divergence of Bov-B LINEs between copies suggests that recent multiple HTs occurred within the same evolutionary timeframe in the snake lineage. The proportion of Bov-B LINEs varies among species, reflecting species specificity in TE invasion. The rapid speciation of snakes, coinciding with Bov-B LINE invasion in snake genomes, leads us to better understand the effect of Bov-B LINEs on snake genome evolution.

Dataset Information

Multiple recent horizontal transfers of a large genomic region in cheese making fungi.

Publications

Multiple recent horizontal transfers of a large genomic region in cheese making fungi.

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