Horizontal Gene Transfer as an Indispensable Driver for Evolution of Neocallimastigomycota into a Distinct Gut-Dwelling Fungal Lineage

ABSTRACTSurvival and growth of the anaerobic gut fungi (AGF; Neocallimastigomycota) in the herbivorous gut necessitate the possession of multiple abilities absent in other fungal lineages. We hypothesized that horizontal gene transfer (HGT) was instrumental in forging the evolution of AGF into a phylogenetically distinct gut-dwelling fungal lineage. The patterns of HGT were evaluated in the transcriptomes of 27 AGF strains, 22 of which were isolated and sequenced in this study, and 4 AGF genomes broadly covering the breadth of AGF diversity. We identified 277 distinct incidents of HGT in AGF transcriptomes, with subsequent gene duplication resulting in an HGT frequency of 2 to 3.5% in AGF genomes. The majority of HGT events were AGF specific (91.7%) and wide (70.8%), indicating their occurrence at early stages of AGF evolution. The acquired genes allowed AGF to expand their substrate utilization range, provided new venues for electron disposal, augmented their biosynthetic capabilities, and facilitated their adaptation to anaerobiosis. The majority of donors were anaerobic fermentative bacteria prevalent in the herbivorous gut. This study strongly indicates that HGT indispensably forged the evolution of AGF as a distinct fungal phylum and provides a unique example of the role of HGT in shaping the evolution of a high-rank taxonomic eukaryotic lineage.IMPORTANCEThe anaerobic gut fungi (AGF) represent a distinct basal phylum lineage (Neocallimastigomycota) commonly encountered in the rumen and alimentary tracts of herbivores. Survival and growth of anaerobic gut fungi in these anaerobic, eutrophic, and prokaryote-dominated habitats necessitates the acquisition of several traits absent in other fungal lineages. We assess here the role of horizontal gene transfer as a relatively fast mechanism for trait acquisition by the Neocallimastigomycota postsequestration in the herbivorous gut. Analysis of 27 transcriptomes that represent the broad diversity of Neocallimastigomycota identified 277 distinct HGT events, with subsequent gene duplication resulting in an HGT frequency of 2 to 3.5% in AGF genomes. These HGT events have allowed AGF to survive in the herbivorous gut by expanding their substrate utilization range, augmenting their biosynthetic pathway, providing new routes for electron disposal by expanding fermentative capacities, and facilitating their adaptation to anaerobiosis. HGT in the AGF is also shown to be mainly a cross-kingdom affair, with the majority of donors belonging to the bacteria. This study represents a unique example of the role of HGT in shaping the evolution of a high-rank taxonomic eukaryotic lineage.

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Horizontal gene transfer as an indispensable driver for Neocallimastigomycota evolution into a distinct gut-dwelling fungal lineage

10.1101/487215 ◽

2018 ◽

Cited By ~ 2

Author(s):

Chelsea L. Murphy ◽

Noha H. Youssef ◽

Radwa A. Hanafy ◽

MB Couger ◽

Jason E. Stajich ◽

...

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Gene Duplication ◽

Substrate Utilization ◽

High Rank ◽

Eukaryotic Lineage ◽

Fungal Lineage ◽

Fermentative Bacteria ◽

Survival And Growth

AbstractSurvival and growth of the anaerobic gut fungi (AGF, Neocallimastigomycota) in the herbivorous gut necessitate the possession of multiple abilities absent in other fungal lineages. We hypothesized that horizontal gene transfer (HGT) was instrumental in forging the evolution of AGF into a phylogenetically distinct gut-dwelling fungal lineage. Patterns of HGT were evaluated in the transcriptomes of 27 AGF strains, 22 of which were isolated and sequenced in this study, and 4 AGF genomes broadly covering the breadth of AGF diversity. We identified 283 distinct incidents of HGT in AGF transcriptomes, with subsequent gene duplication resulting in an HGT frequency of 2.1-3.6% in AGF genomes. The majority of HGT events were AGF specific (91.5%) and wide (70.7%), indicating their occurrence at early stages of AGF evolution. The acquired genes allowed AGF to expand their substrate utilization range, provided new venues for electron disposal, augmented their biosynthetic capabilities, and facilitated their adaptation to anaerobiosis. The majority of donors were anaerobic fermentative bacteria prevalent in the herbivorous gut. This work strongly indicates that HGT indispensably forged the evolution of AGF as a distinct fungal phylum and provides a unique example of the role of HGT in shaping the evolution of a high rank taxonomic eukaryotic lineage.ImportanceThe anaerobic gut fungi (AGF) represent a distinct basal phylum lineage (Neocallimastigomycota) commonly encountered in the rumen and alimentary tracts of herbivores. Survival and growth of anaerobic gut fungi in these anaerobic, eutrophic, and prokaryotes dominated habitats necessitates the acquisition of several traits absent in other fungal lineages. This manuscript assesses the role of horizontal gene transfer as a relatively fast mechanism for trait acquisition by the Neocallimastigomycota post sequestration in the herbivorous gut. Analysis of twenty-seven transcriptomes that represent the broad Neocallimastigomycota diversity identified 283 distinct HGT events, with subsequent gene duplication resulting in an HGT frequency of 2.1-3.6% in AGF genomes. These HGT events have allowed AGF to survive in the herbivorous gut by expanding their substrate utilization range, augmenting their biosynthetic pathway, providing new routes for electron disposal by expanding fermentative capacities, and facilitating their adaptation to anaerobiosis. HGT in the AGF is also shown to be mainly a cross-kingdom affair, with the majority of donors belonging to the bacteria. This work represents a unique example of the role of HGT in shaping the evolution of a high rank taxonomic eukaryotic lineage.

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Detection of Listeria Spp. During Production and Ripening of Petrovská Klobása/Detekcija Listeria Spp. U Toku Proizvodnje I Zrenja Petrovačke Kobasice

Acta veterinaria ◽

10.2478/acve-2014-0035 ◽

2014 ◽

Vol 64 (3) ◽

pp. 367-377 ◽

Cited By ~ 2

Author(s):

Lakićević Brankica ◽

Bunčić Olivera ◽

Katić Vera ◽

Lepšanović Zorica ◽

Petrović Ljiljana ◽

...

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Water Activity ◽

Genome Sequence ◽

Starter Culture ◽

Activity Temperature ◽

Survival And Growth ◽

Hlya Gene ◽

And Storage

Abstract The aim of this study was to determine the survival of Listeria spp. during the preparation and ripening of an artisan Serbian sausage (Petrovská klobása) and to characterize the isolates by amplification of the hlyA gene. Results obtained by standard microbiological and molecular methods showed that during fermentation, drying, ripening and storage of Petrovská klobása, 17 out of 99 samples were positive for the presence of Listeria spp. Among them we detected a hemolytic, atypical, non pathogenic L. innocua strain FSL J1-023, whose genome sequence is important in understanding the role of horizontal gene transfer and recombination in the evolution of pathogenicity of Listeria. The most important product characteristics influencing the survival and growth of Listeria spp. during production and ripening of Petrovská klobása were: pH, water activity, temperature and starter culture.

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Horizontal Gene Transfer Involving Chloroplasts

International Journal of Molecular Sciences ◽

10.3390/ijms22094484 ◽

2021 ◽

Vol 22 (9) ◽

pp. 4484

Author(s):

Ewa Filip ◽

Lidia Skuza

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Driving Force ◽

Genetic Material ◽

Adaptive Significance ◽

Chloroplast Genomes ◽

Organelle Genomes ◽

Number Of Genes ◽

Cellular Compartments

Horizontal gene transfer (HGT)- is defined as the acquisition of genetic material from another organism. However, recent findings indicate a possible role of HGT in the acquisition of traits with adaptive significance, suggesting that HGT is an important driving force in the evolution of eukaryotes as well as prokaryotes. It has been noted that, in eukaryotes, HGT is more prevalent than originally thought. Mitochondria and chloroplasts lost a large number of genes after their respective endosymbiotic events occurred. Even after this major content loss, organelle genomes still continue to lose their own genes. Many of these are subsequently acquired by intracellular gene transfer from the original plastid. The aim of our review was to elucidate the role of chloroplasts in the transfer of genes. This review also explores gene transfer involving mitochondrial and nuclear genomes, though recent studies indicate that chloroplast genomes are far more active in HGT as compared to these other two DNA-containing cellular compartments.

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