Several steps of lateral gene transfer followed by events of ‘birth-and-death’ evolution shaped a fungal sorbicillinoid biosynthetic gene cluster

Abstract

BackgroundSorbicillinoids are a family of complex cyclic polyketides produced by only a small number of distantly related ascomycete fungi such as Trichoderma (Sordariomycetes) and Penicillium (Eurotiomycetes). In T. reesei, they are synthesized by a gene cluster consisting of eight genes including two polyketide synthases (PKS). To reconstruct the evolutionary origin of this gene cluster, we examined the occurrence of these eight genes in ascomycetes.ResultsA cluster comprising at least six of them was only found in Hypocreales (Acremonium chrysogenum, Ustilaginoidea virens, Trichoderma species from section Longibrachiatum) and in Penicillium rubens (Eurotiales). In addition, Colletotrichum graminicola contained the two pks (sor1 and sor2), but not the other sor genes. A. chrysogenum was the evolutionary eldest species in which sor1, sor2, sor3, sor4 and sor6 were present. Sor5 was gained by lateral gene transfer (LGT) from P. rubens. In the younger Hypocreales (U. virens, Trichoderma spp.), the cluster evolved by vertical transfer, but sor2 was lost and regained by LGT from C. graminicola. SorB (=sor2) and sorD (=sor4) were symplesiomorphic in P. rubens, whereas sorA, sorC and sorF were obtained by LGT from A. chrysogenum, and sorE by LGT from Pestalotiopsis fici (Xylariales). The sorbicillinoid gene cluster in Trichoderma section Longibrachiatum is under strong purifying selection. The T. reesei sor genes are expressed during fast vegetative growth, during antagonism of other fungi and regulated by the secondary metabolism regulator LAE1.ConclusionsOur findings pinpoint the evolution of the fungal sorbicillinoid biosynthesis gene cluster. The core cluster arose in early Hypocreales, and was complemented by LGT. During further speciation in the Hypocreales, it became subject to birth and death evolution in selected lineages. In P. rubrens (Eurotiales), two cluster genes were symplesiomorphic, and the whole cluster formed by LGT from at least two different fungal donors.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0834-6) contains supplementary material, which is available to authorized users.

Constitutive hyperproduction of sorbicillinoids in Trichoderma reesei ZC121

“…Genes involved in the biosynthesis of sorbicillinoids were clustered in the T. reesei genome and named the “sorbicillinoid gene cluster” [ 14 , 25 ]. This T. reesei gene cluster contains a highly reducing PKS Sor 1, a non-reducing PKS Sor 2, a flavin adenine dinucleotide (FAD)-dependent monooxygenase Sor3, a FAD/flavin mononucleotide-containing dehydrogenase Sor4, two transcription factors YPR1 and YPR2 [ 3 ], a MFS transporter Sor6, and a short-chain dehydrogenase/reductase Sor 5 (Fig.…”

“…7 b and Additional file 1 : Table S2). Gene sor5 in this study, which is designated as sor7 in the literature, encodes a short-chain dehydrogenase/reductase [ 14 ]. Its ortholog from P. rubens was not located in the sorbicillinoid gene cluster.…”

“…The heterotrimeric velvet complex VelB/VeA/LaeA correlates fungal development and secondary metabolism in response to light. Moreover, it is found that both the knockout and overexpression of gene laeA affected the expression of some sor genes [ 14 ]. Nevertheless, the mRNA level of all these three genes remained unchanged in strain ZC121 in comparison with RUT-C30.…”

“…Sorbicillinoids, also termed “yellow pigment,” are derived from PKS and a large group of hexaketide secondary metabolites and include the cyclization on the carboxylate terminus. Sorbicillinoids are produced and secreted by both marine and terrestrial ascomycetes, including Trichoderma [ 9 ], Aspergillus [ 10 ], Penicillium [ 11 ], Streptomyces [ 1 ], Acremonium [ 12 ], Paecilomyces [ 13 ], and Eurotiomycete [ 14 ]. Most of these compounds possess the characteristic C1–C6 sorbyl sidechain and bi- or tri-cyclic frameworks that are extremely complex and highly oxygenated.…”

Gene regulation associated with sexual development and female fertility in different isolates of Trichoderma reesei

“…Among the transcription factor genes, a homologue of the N. crassa grainy head like transcription factor encoding csp - 2 , which is involved in conidial separation, development and cell wall remodeling [ 34 ], was found. However, the most interesting finding was the high level transcription of the three biosynthetic genes of the recently described SOR cluster [ 23 , 33 , 35 ] with TR_73618/ sor2/pks10s , TR_73621/ sor1/pks11s and TR73623/ sor5 being among the 10 genes with highest overall transcript levels in CBS999.97. We therefore tested transcript abundance of sor1 under conditions of sexual development (contact stage, before fruiting body formation) compared to cellulose (Fig.…”