A robust phylogenomic timetree for biotechnologically and medically important fungi in the genera Aspergillus and Penicillium

Abstract

The 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.Penicillium expansum, Penicillium digitatum, and Penicillium italicum (Marcet-Houben et al. 2012;Ballester et al. 2015;Li et al. 2015).

Characterizing gene tree conflict in plastome-inferred phylogenies

“…In light of our results, rpoC2 should be a highly attractive coding region for future studies, as it generally recapitulates the plastome phylogeny while allowing more proper branch length inferences (given that conflicting signal among multiple genes can result in problematic branch length estimates: Mendes & Hahn, 2016). Recent work (Salichos & Rokas, 2013; Smith, Brown & Walker, 2018; Steenwyk et al, 2018) indicates that filtering for a smaller set of highly informative genes might yield more accurate results in various phylogenetic applications (e.g., topology estimation, divergence dating). Given this, rpoC2 might be particularly useful for comparative analyses requiring accurate branch length estimates (i.e., the majority of comparative analyses).…”

“…Even if the concatenated topology is largely congruent with the ‘true’ species tree of a given group, underlying conflict can mislead branch length estimation (Mendes & Hahn, 2016). Therefore, we recommend that comparative methods and/or dating analyses that rely on branch lengths use filtering procedures similar to those proposed for nuclear data (Salichos & Rokas, 2013; Smith, Brown & Walker, 2018; Steenwyk et al, 2018).…”

Characterizing the Pathogenic, Genomic, and Chemical Traits of Aspergillus fischeri , a Close Relative of the Major Human Fungal Pathogen Aspergillus fumigatus

“…turcosus) (1, 44, 78, 79). The ability to cause disease in humans appears to have either arisen or been lost (or both) multiple times independently during the evolution of this lineage, as pathogenic species are spread throughout the phylogeny (17, 80). A broader, phylogenetically informed comparison of pathogenic and nonpathogenic species in section Fumigati would provide far greater resolution in identifying (or dismissing) factors and pathways that may contribute to or prevent the ability of these organisms to cause disease.…”

“…For example, Aspergillusfischeri is the closest evolutionary relative to A. fumigatus for which a genome has been sequenced (16, 17), but it is rarely reported to cause human disease (1). Recent evolutionary genomic analyses suggest that A. fischeri and A.…”

“…Recent evolutionary genomic analyses suggest that A. fischeri and A. fumigatus last shared a common ancestor approximately 4 million years ago (95% credible interval: 2 to 7 million years ago) (17). Why A. fischeri -mediated disease is less common than A.…”