Biology subjects

Shen, X.-X.

Publications and source records attributed to Shen, X.-X..

5 recordsLinked to original sources

bioRxiv2018

Eukaryotic acquisition of a bacterial operon

Operons are a hallmark of bacterial genomes, where they allow concerted expression of multiple functionally related genes as single polycistronic transcripts. They are rare in eukaryotes, where each gene usually drives expression of its own independent messenger RNAs. Here we report the horizontal operon transfer of a catecholate-class siderophore biosynthesis pathway from Enterobacteriaceae into a group of closely related yeast taxa. We further show that the co-linearly arranged secondary metabolism genes are actively expressed, exhibit mainly eukaryotic transcriptional features, and enable the sequestration and uptake of iron. After transfer to the eukaryotic host, several genetic changes occurred, including the acquisition of polyadenylation sites, structural rearrangements, integration of eukaryotic genes, and secondary loss in some lineages. We conclude that the operon genes were likely captured in the shared insect gut habitat, modified for eukaryotic gene expression, and maintained by selection to adapt to the highly-competitive, iron-limited environment.

evolutionary biology↗

bioRxiv2018

A robust phylogenomic timetree for biotechnologically and medically important fungi from Aspergillaceae (Eurotiomycetes, Ascomycota)

AbbreviationsNT, nucleotide; AA, amino acid; CI, credible interval; RCV, relative composition variability; IC, internode certainty; GSF, gene support frequencies; GLS, gene-wise log-likelihood scores; DVMC, degree of violation of a molecular clock\n\nThe filamentous fungal family Aspergillaceae contains > 1,000 known species, mostly in the genera Aspergillus and Penicillium. Several species are used in the food, biotechnology, and drug industries (e.g., Aspergillus oryzae, Penicillium camemberti), while others are dangerous human and plant pathogens (e.g., Aspergillus fumigatus, Penicillium digitatum). To infer a robust phylogeny and pinpoint poorly resolved branches and their likely underlying contributors, we used 81 genomes spanning the diversity of Aspergillus and Penicillium to construct a 1,668-gene data matrix. Phylogenies of the nucleotide and amino acid versions of this full data matrix as well as of five additional 834-gene data matrices constructed by subsampling the top 50% of genes according to different criteria associated with strong phylogenetic signal were generated using three different maximum likelihood schemes (i.e., gene-partitioned, unpartitioned, and coalescence). Examination of the topological agreement among these 36 phylogenies and measures of internode certainty identified 12 / 78 (15.4%) bipartitions that were incongruent and pinpoint the likely underlying contributing factors (incomplete lineage sorting, hybridization or introgression, and reconstruction artifacts associated with poor taxon sampling). Relaxed molecular clock analyses suggest that Aspergillaceae likely originated in the lower Cretaceous and the Aspergillus and Penicillium genera in the upper Cretaceous. Our results shed light on the ongoing debate on Aspergillus systematics and taxonomy and provide a robust evolutionary and temporal framework for comparative genomic analyses in Aspergillaceae. More broadly, our approach provides a general template for phylogenomic identification of resolved and contentious branches in densely genome-sequenced lineages across the tree of life.

evolutionary biology↗

bioRxiv2017

Evidence for loss and adaptive reacquisition of alcoholic fermentation in an early-derived fructophilic yeast lineage

Fructophily is a rare trait that consists in the preference for fructose over other carbon sources. Here we show that in a yeast lineage (the Wickerhamiella/Starmerella, W/S clade) formed by fructophilic species thriving in the floral niche, the acquisition of fructophily is part of a wider process of adaptation of central carbon metabolism to the high sugar environment. Coupling comparative genomics with biochemical and genetic approaches, we show that the alcoholic fermentation pathway was profoundly remodeled in the W/S clade, as genes required for alcoholic fermentation were lost and subsequently re-acquired from bacteria through horizontal gene transfer. We further show that the reinstated fermentative pathway is functional and that an enzyme required for sucrose assimilation is also of bacterial origin, reinforcing the adaptive nature of the genetic novelties identified in the W/S clade. This work shows how even central carbon metabolism can be remodeled by a surge of HGT events.

genomics↗

bioRxiv2017

Genomic features and evolution of the conditionally dispensable chromosome in the tangerine pathotype of Alternaria alternata

The tangerine pathotype of the ascomycete fungus Alternaria alternata is the causal agent of citrus brown spot, which can result in significant losses of both yield and marketability for tangerines and tangerine hybrids worldwide. A conditionally dispensable chromosome (CDC), which harbors the host-selective ACT toxin gene cluster, is required for tangerine pathogenicity of A. alternata. To understand the genetic makeup and evolution of the tangerine pathotype CDC, we analyzed the function and evolution of the CDC genes present in the A. alternata Z7 strain. The 1.84Mb long CDC contains 512 predicted protein-coding genes, which are enriched in functional categories associated with metabolic process (132 genes, p-value = 0.00192) including oxidation-reduction process (48 genes, p-value = 0.00021) and lipid metabolic process (11 genes, p-value = 0.04591). Relatively few of the CDC genes can be classified as CAZymes (13), kinases (3) and transporters (20). Differential transcriptome analysis of H2O2 treatment and control conditions revealed that 29 CDC genes were significantly up-regulated and 14 were significantly down-regulated, suggesting that CDC genes may play a role in coping with oxidative stress. Evolutionary analysis of the 512 CDC proteins showed that their evolutionary conservation tends to be restricted within the genus Alternaria and that the CDC genes evolve faster than genes in the essential chromosomes. Interestingly, phylogenetic analysis suggested that the genes of 13 enzymes and one sugar transporter residing in the CDC were likely horizontally transferred from distantly related species. Among these, one carboxylesterase gene was transferred from bacteria but functionally knocking out this gene revealed no obvious biological role. Another 4 genes might have been transferred from Colletotrichum (Sordariomycetes) and 5 were likely transferred as a physically linked cluster of genes from Cryptococcus (Basidiomycota) or Penicillium (Eurotiomycetes). Functionally knocking out the 5-gene cluster resulted in an 80% decrease in asexual spore production in the deletion mutant. These results provide new insights into the function and evolution of CDC genes in Alternaria.\n\nAuthor SummaryMany fungal phytopathogens harbor conditionally dispensable chromosomes (CDCs). CDCs are variable in size, contain many genes involved in virulence, but their evolution remains obscure. In this study, we investigated the origin of the CDC present in the tangerine pathotype of Alternaria alternata Z7 strain. We found that most of the Z7 CDC proteins are highly conserved within the genus Alternaria but poorly conserved outside the genus. We also discovered that a small number of genes originated via horizontal gene transfer (HGT) from distantly related fungi and bacteria. These horizontally transferred genes include a carboxylesterase gene that was likely acquired from bacteria, a cluster of 4 physically linked genes likely transferred from Colletotrichum, and a cluster of 5 physically linked genes likely transferred from Cryptococcus (Basidiomycota) or Penicillium (Eurotiomycetes). To gain insight into the functions of these transferred genes, we knocked out the bacterial carboxylesterase and the 5-gene cluster. Whereas the carboxylesterase deletion mutant showed no obvious phenotype, the 5-gene cluster mutant showed a dramatically reduced production of asexual spores (conidia). The results of our study suggest that Alternaria CDCs are largely comprised from rapidly evolving native genes; although only a few genes were acquired via horizontal gene transfer, some of them appear to be involved in functions critical to the phytopathogenic lifestyle.

microbiology↗

bioRxiv2017

Evaluating Fast Maximum Likelihood-Based Phylogenetic Programs Using Empirical Phylogenomic Data Sets

Phylogenetics has witnessed dramatic increases in the sizes of data matrices assembled to resolve branches of the tree of life, motivating the development of programs for fast, yet accurate, inference. For example, several different fast programs have been developed in the very popular maximum likelihood framework, including RAxML/ExaML, PhyML, IQ-TREE, and FastTree. Although these four programs are widely used, a systematic evaluation and comparison of their performance using empirical genome-scale data matrices has so far been lacking. To address this question, we evaluated these four programs on 19 empirical phylogenomic data sets from diverse animal, plant, and fungal lineages with respect to likelihood maximization, tree topology, and computational speed. For single-gene tree inference, we found that the more exhaustive and slower strategies (ten searches per alignment) outperformed faster strategies (one tree search per alignment) using RAxML, PhyML, or IQ-TREE. Interestingly, single-gene trees inferred by the three programs yielded comparable coalescent-based species tree estimations. For concatenation-based species tree inference, IQ-TREE consistently achieved the best-observed likelihoods for all data sets, and RAxML/ExaML was a close second. In contrast, PhyML often failed to complete concatenation-based analyses, whereas FastTree was the fastest but generated lower likelihood values and more dissimilar tree topologies in both types of analyses. Finally, data matrix properties, such as the number of taxa and the strength of phylogenetic signal, sometimes substantially influenced the relative performance of the programs. Our results provide real-world gene and species tree phylogenetic inference benchmarks to inform the design and execution of large-scale phylogenomic data analyses.

evolutionary biology↗