Abstract
High affinity nitrate assimilation genes in fungi occur in a cluster (fHANT-AC) that can be coordinately regulated. The clustered genes include nrt2, which codes for a high affinity nitrate transporter; euknr, which codes for nitrate reductase; and NAD(P)H-nir, which codes for nitrite reductase. Homologs of genes in the fHANT-AC occur in other eukaryotes and prokaryotes, but they have only been found clustered in the oomycete Phytophthora (heterokonts). We performed independent and concatenated phylogenetic analyses of homologs of all three genes in the fHANT-AC. Phylogenetic analyses limited to fungal sequences suggest that the fHANT-AC has been transferred horizontally from a basidiomycete (mushrooms and smuts) to an ancestor of the ascomycetous mold Trichoderma reesei. Phylogenetic analyses of sequences from diverse eukaryotes and eubacteria, and cluster structure, are consistent with a hypothesis that the fHANT-AC was assembled in a lineage leading to the oomycetes and was subsequently transferred to the Dikarya (Ascomycota+Basidiomycota), which is a derived fungal clade that includes the vast majority of terrestrial fungi. We propose that the acquisition of high affinity nitrate assimilation contributed to the success of Dikarya on land by allowing exploitation of nitrate in aerobic soils, and the subsequent transfer of a complete assimilation cluster improved the fitness of T. reesei in a new niche. Horizontal transmission of this cluster of functionally integrated genes supports the “selfish operon” hypothesis for maintenance of gene clusters.
Highlights
A cluster of nitrate assimilation genes occurs in the ascomycetes Aspergillus nidulans [1] and Pichia angusta [2] and in the basidiomycetes Hebeloma cylindrosporum, which is mycorrhizal, and Phanerochaete chrysosporium [3], which is a wood-decayer
Homologs of each of the three genes of the fHANT-AC (SI Table S1) are limited to Viridiplantae, Rhodophyta, heterokonts and Dikarya, with one exception in Nematostella vectensis (Metazoa), which possesses bacteria-like nrt2 and nitrite reductase homologs
A Shimodaira-Hasegawa test (Table 1) rejected the monophyly of ascomycete nitrate assimilation clusters when T. reesei sequences were included (p,0.0001). These analyses indicate strong conflict between the organismal and nitrate assimilation gene phylogenies that is best explained by horizontal gene transfer (HGT) of the fHANTAC from the Ustilaginales to Trichoderma
Summary
A cluster of nitrate assimilation genes occurs in the ascomycetes Aspergillus nidulans [1] and Pichia angusta [2] and in the basidiomycetes Hebeloma cylindrosporum, which is mycorrhizal, and Phanerochaete chrysosporium [3], which is a wood-decayer This cluster, abbreviated fHANT-AC, encodes a high affinity nitrate transporter (NRT2, TCDB 2.A.1.8.5) along with a nitrate reductase (EUKNR, EC1.7.1.3) and a ferredoxin-independent assimilatory nitrite reductase (NAD[P]H-NIR, EC1.7.1.4). Nrt is widely distributed in bacteria, plants, heterokonts and other groups, but not in opisthokonts outside Dikarya [5]. Euknr is restricted to eukaryotes, and absent from opisthokonts outside Dikarya, and NAD(P)H-nir is known to occur in Dikarya, heterokonts and bacteria
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
