scholarly journals Genome organization and evolution of a eukaryotic nicotinate co-inducible pathway

Open Biology ◽  
2021 ◽  
Vol 11 (9) ◽  
Author(s):  
Eszter Bokor ◽  
Michel Flipphi ◽  
Sándor Kocsubé ◽  
Judit Ámon ◽  
Csaba Vágvölgyi ◽  
...  

In Aspergillus nidulans a regulon including 11 hxn genes ( hxnS , T , R , P , Y , Z , X , W , V , M and N ) is inducible by a nicotinate metabolic derivative, repressible by ammonium and under stringent control of the nitrogen-state-sensitive GATA factor AreA and the specific transcription factor HxnR. This is the first report in a eukaryote of the genomic organization of a possibly complete pathway of nicotinate utilization. In A. nidulans the regulon is organized in three distinct clusters, this organization is variable in the Ascomycota . In some Pezizomycotina species all 11 genes map in a single cluster; in others they map in two clusters. This variable organization sheds light on cluster evolution. Instances of gene duplication followed by or simultaneous with integration in the cluster, partial or total cluster loss, and horizontal gene transfer of several genes (including an example of whole cluster re-acquisition in Aspergillus of section Flavi ) were detected, together with the incorporation in some clusters of genes not found in the A. nidulans co-regulated regulon, which underlie both the plasticity and the reticulate character of metabolic cluster evolution. This study provides a comprehensive phylogeny of six members of the cluster across representatives of all Ascomycota classes.

2021 ◽  
Author(s):  
Eszter Bokor ◽  
Michel Flipphi ◽  
Sandor Kocsube ◽  
Judit Amon ◽  
Csaba Vagvolgyi ◽  
...  

We describe an HxnR-dependent regulon composed of 11 hxn genes (hxnS, T, R, P, Y, Z, X, W, V, M and N). The regulon is inducible by a nicotinate metabolic derivative and repressible by ammonium and under stringent control of the GATA factor AreA. This is the first publication of a eukaryotic, complete nicotinate metabolic cluster including five novel genes. While in A. nidulans the regulon is organised in three distinct clusters, this organisation is variable in the Ascomycota. In some Pezizomycotina species all the 11 genes are organised in a single cluster, in other in two clusters. This variable organisation sheds light on cluster evolution. Instances of gene duplication, followed by or simultaneous with integration in the cluster; partial or total cluster loss; horizontal gene transfer of several genes, including an example of whole cluster re-acquisition in Aspergillus of section Flavi were detected, together with the incorporation in some clusters of genes not found in the A. nidulans co-regulated regulon, which underlie both the plasticity and the reticulate character of metabolic cluster evolution. This study provides the first comprehensive protein sequence comparison of six members of the cluster across representatives of all Ascomycota classes, including several hundreds of species.


2017 ◽  
Author(s):  
Revathy Krishnamurthi ◽  
Swagatha Ghosh ◽  
Supriya Khedkar ◽  
Aswin Sai Narain Seshasayee

AbstractHorizontal gene transfer is a major driving force behind the genomic diversity seen in prokaryotes. Theracprophage inE.coliK12 encodes a putative transcription factor RacR, whose deletion is lethal. We have shown that the essentiality ofracRinE.coliK12 is attributed to its role in transcriptionally repressing a toxin gene calledydaS, which is coded adjacent and divergently toracR.


2018 ◽  
Author(s):  
Chelsea L. Murphy ◽  
Noha H. Youssef ◽  
Radwa A. Hanafy ◽  
MB Couger ◽  
Jason E. Stajich ◽  
...  

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.


2018 ◽  
Author(s):  
Peter Thorpe ◽  
Carmen M. Escudero-Martinez ◽  
Peter J. A. Cock ◽  
D. Laetsch ◽  
Sebastian Eves-van den Akker ◽  
...  

AbstractBackgroundAphids are a diverse group of taxa that contain hundreds of agronomically important species, which vary in their host range and pathogenicity. However, the genome evolution underlying agriculturally important aphid traits is not well understood.ResultsWe generated highly-contiguous draft genome assemblies for two aphid species: the narrow host range Myzus cerasi, and the cereal specialist Rhopalosiphum padi. Using a de novo gene prediction pipeline on both these genome assemblies, and those of three related species (Acyrthosiphon pisum, D. noxia and M. persicae), we show that aphid genomes consistently encode similar gene numbers, and in the case of A. pisum, fewer and larger genes than previously reported. We compare gene content, gene duplication, synteny, horizontal gene transfer events, and putative effector repertoires between these five species to understand the genome evolution of globally important plant parasites.Aphid genomes show signs of relatively distant gene duplication, and substantial, relatively recent, gene birth, and are characterized by disparate gain and loss of genes acquired by horizontal gene transfer (HGT). Such HGT events account for approximately 1% of loci, and contribute to the protein-coding content of aphid species analysed. Putative effector repertoires, originating from duplicated loci, putative HGT events and other loci, have an unusual genomic organisation and evolutionary history. We identify a highly conserved effector-pair that is tightly genetically-linked in all aphid species. In R. padi, this effector pair is tightly transcriptionally-linked, and shares a transcriptional control mechanism with a subset of approximately 50 other putative effectors distributed across the genome.ConclusionsThis study extends our current knowledge on the evolution of aphid genomes and reveals evidence for a shared control mechanism, which underlies effector expression, and ultimately plant parasitism.


2019 ◽  
Vol 85 (15) ◽  
Author(s):  
Chelsea L. Murphy ◽  
Noha H. Youssef ◽  
Radwa A. Hanafy ◽  
M. B. Couger ◽  
Jason E. Stajich ◽  
...  

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.


2020 ◽  
Vol 12 (11) ◽  
pp. 2168-2182
Author(s):  
Yen-Wen Wang ◽  
Jaqueline Hess ◽  
Jason C Slot ◽  
Anne Pringle

Abstract By introducing novel capacities and functions, new genes and gene families may play a crucial role in ecological transitions. Mechanisms generating new gene families include de novo gene birth, horizontal gene transfer, and neofunctionalization following a duplication event. The ectomycorrhizal (ECM) symbiosis is a ubiquitous mutualism and the association has evolved repeatedly and independently many times among the fungi, but the evolutionary dynamics enabling its emergence remain elusive. We developed a phylogenetic workflow to first understand if gene families unique to ECM Amanita fungi and absent from closely related asymbiotic species are functionally relevant to the symbiosis, and then to systematically infer their origins. We identified 109 gene families unique to ECM Amanita species. Genes belonging to unique gene families are under strong purifying selection and are upregulated during symbiosis, compared with genes of conserved or orphan gene families. The origins of seven of the unique gene families are strongly supported as either de novo gene birth (two gene families), horizontal gene transfer (four), or gene duplication (one). An additional 34 families appear new because of their selective retention within symbiotic species. Among the 109 unique gene families, the most upregulated gene in symbiotic cultures encodes a 1-aminocyclopropane-1-carboxylate deaminase, an enzyme capable of downregulating the synthesis of the plant hormone ethylene, a common negative regulator of plant-microbial mutualisms.


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