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Niche differentiation and evolution of the wood decay machinery in the invasive fungus Serpula lacrymans.

ABSTRACT: Ecological niche breadth and the mechanisms facilitating its evolution are fundamental to understanding adaptation to changing environments, persistence of generalist and specialist lineages and the formation of new species. Woody substrates are structurally complex resources utilized by organisms with specialized decay machinery. Wood-decaying fungi represent ideal model systems to study evolution of niche breadth, as they vary greatly in their host range and preferred decay stage of the substrate. In order to dissect the genetic basis for niche specialization in the invasive brown rot fungus Serpula lacrymans, we used phenotyping and integrative analysis of phylogenomic and transcriptomic data to compare this species to wild relatives in the Serpulaceae with a range of specialist to generalist decay strategies. Our results indicate specialist species have rewired regulatory networks active during wood decay towards decreased reliance on enzymatic machinery, and therefore nitrogen-intensive decay components. This shift was likely accompanied with adaptation to a narrow tree line habitat and switch to a pioneer decomposer strategy, both requiring rapid colonization of a nitrogen-limited substrate. Among substrate specialists with narrow niches, we also found evidence for pathways facilitating reversal to generalism, highlighting how evolution may move along different axes of niche space.

SUBMITTER: Hess J

PROVIDER: S-EPMC8027034 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Cytochrome P450 Complement May Contribute to Niche Adaptation in Serpula Wood-Decay Fungi.

Project description:Serpula wood-decay fungi occupy a diverse range of natural and man-made ecological niches. Serpula himantioides is a forest-floor generalist with global coverage and strong antagonistic ability, while closely related species Serpula lacrymans contains specialist sister strains with widely differing ecologies. Serpula lacrymans var. shastensis is a forest-floor specialist in terms of resource preference and geographic coverage, while Serpula lacrymans var. lacrymans has successfully invaded the built environment and occupies a building-timber niche. To increase understanding of the cellular machinery required for niche adaptation, a detailed study of the P450 complement of these three strains was undertaken. Cytochrome P450 monooxygenases are present in all fungi and typically seen in high numbers in wood decay species, with putative roles in breakdown of plant extractives and lignocellulose metabolism. Investigating the genomes of these related yet ecologically diverse fungi revealed a high level of concordance in P450 complement, but with key differences in P450 family representation and expression during growth on wood, suggesting P450 proteins may play a role in niche adaptation. Gene expansion of certain key P450 families was noted, further supporting an important role for these proteins during wood decay. The generalist species S. himantioides was found to have the most P450 genes with the greatest family diversity and the highest number of P450 protein families expressed during wood decay.

| S-EPMC8949155 | biostudies-literature

Microbiota Associated with Different Developmental Stages of the Dry Rot Fungus Serpula lacrymans.

Project description:The dry rot fungus Serpula lacrymans causes significant structural damage by decaying construction timber, resulting in costly restoration procedures. Dry rot fungi decompose cellulose and hemicellulose and are often accompanied by a succession of bacteria and other fungi. Bacterial-fungal interactions (BFI) have a considerable impact on all the partners, ranging from antagonistic to beneficial relationships. Using a cultivation-based approach, we show that S. lacrymans has many co-existing, mainly Gram-positive, bacteria and demonstrate differences in the communities associated with distinct fungal parts. Bacteria isolated from the fruiting bodies and mycelia were dominated by Firmicutes, while bacteria isolated from rhizomorphs were dominated by Proteobacteria. Actinobacteria and Bacteroidetes were less abundant. Fluorescence in situ hybridization (FISH) analysis revealed that bacteria were not present biofilm-like, but occurred as independent cells scattered across and within tissues, sometimes also attached to fungal spores. In co-culture, some bacterial isolates caused growth inhibition of S. lacrymans, and vice versa, and some induced fungal pigment production. It was found that 25% of the isolates could degrade pectin, 43% xylan, 17% carboxymethylcellulose, and 66% were able to depolymerize starch. Our results provide first insights for a better understanding of the holobiont S. lacrymans and give hints that bacteria influence the behavior of S. lacrymans in culture.

| S-EPMC8147175 | biostudies-literature

Serpula lacrymans gene expression on different substrates

Project description:Transcript profiles of Serpula lacrymans grown on different substrates were analyzed. The array probes were designed from gene models taken from the Joint Genome Institute (JGI, department of energy) Serpula lacrymans genome sequence version 1. One aim of this study was to verify the expression of the automatically annotated gene models under various conditions. Another goal was to compare gene expression profiles from Serpula lacrymans grown on liquid MMN medium and on wood.

2011-07-01 | GSE27839 | GEO

Biochemical characterization of Serpula lacrymans iron-reductase enzymes in lignocellulose breakdown.

Project description:Putative iron-reductase (IR) genes from Serpula lacrymans with similarity to the conserved iron-binding domains of cellobiose dehydrogenase (CDH) enzymes have been identified. These genes were cloned and expressed to functionally characterize their activity and role in the decomposition of lignocellulose. The results show that IR1 and IR2 recombinant enzymes have the ability to depolymerize both lignin and cellulose, are capable of the reduction of ferric iron to the ferrous form, and are capable of the degradation of nitrated lignin. Expression of these genes during wheat straw solid-state fermentation was shown to correlate with the release of compounds associated with lignin decomposition. The results suggest that both IR enzymes mediate a non-enzymatic depolymerisation of lignocellulose and highlight the potential of chelator-mediated Fenton systems in the industrial pre-treatment of biomass.

| S-EPMC6971154 | biostudies-literature

High variability in a mating type linked region in the dry rot fungus Serpula lacrymans caused by frequency-dependent selection?

Project description:BackgroundThe mating type loci that govern the mating process in fungi are thought to be influenced by negative frequency-dependent selection due to rare allele advantage. In this study we used a mating type linked DNA marker as a proxy to indirectly study the allelic richness and geographic distribution of mating types of one mating type locus (MAT A) in worldwide populations of the dry rot fungus Serpula lacrymans. This fungus, which causes serious destruction to wooden constructions in temperate regions worldwide, has recently expanded its geographic range with a concomitant genetic bottleneck.ResultsHigh allelic richness and molecular variation was detected in the mating type linked marker as compared to other presumably neutral markers. Comparable amounts of genetic variation appeared in the mating type linked marker in populations from nature and buildings, which contrast the pattern observed with neutral genetic markers where natural populations were far more variable. Some geographic structuring of the allelic variation in the mating type linked marker appeared, but far less than that observed with neutral markers. In founder populations of S. lacrymans, alleles co-occurring in heterokaryotic individuals were more divergent than expected by chance, which agrees with the expectation for populations where few mating alleles exists. The analyzed DNA marker displays trans-species polymorphism wherein some alleles from the closely related species S. himantoides are more similar to those of S. lacrymans than other alleles from S. himantoides.ConclusionsOur results support the idea that strong negative frequency-dependent selection maintains high levels of genetic variation in MAT-linked genomic regions, even in recently bottlenecked populations of S. lacrymans.

| S-EPMC2909151 | biostudies-literature

Serpula lacrymans

Project description:Genome sequencing and assembly of Serpula lacrymans var. lacrymans and Serpula lacrymans var. shastensis

| PRJNA412961 | ENA

Serpula lacrymans

Project description:Fungus that causes dry rot in wood building constructions

| PRJNA32887 | ENA

Fungus wars: basidiomycete battles in wood decay.

Project description:Understanding the mechanisms underlying wood decay basidiomycete community dynamics is crucial for fully understanding decomposition processes, and for modelling ecosystem function and resilience to environmental change. Competition drives community development in decaying woody resources, with interactions occurring at a distance, following physical contact, and through specialised relationships such as mycoparasitism. Outcomes of combative interactions range from replacement, where one mycelium displaces another, to deadlock, where neither combatant captures territory from the other; and a spectrum of intermediate outcomes (i.e. partial or mutual replacement) lie between these extremes. Many wood decay basidiomycetes coexist within a resource, in a complex and dynamic community, and new research techniques are focussing on spatial orientation of interactions in 3 dimensions, as opposed to historical two-dimensional research. Not only do interactions drive changes in species composition and thus wood decomposition rate, they also may have industrial applications in biocontrol of pathogenic or nuisance fungi, enzyme production, and in the production of novel antifungals and antibiotics. Altogether, fungal interactions are a fascinating and important field of study.

| S-EPMC6002336 | biostudies-literature

Serpula lacrymans var. lacrymans

Project description:Contrasting demographic histories revealed in two invasive populations of the dry rot fungus Serpula lacrymans

| PRJNA685018 | ENA

Molecular characterization of sexual diversity in a population of Serpula lacrymans, a tetrapolar basidiomycete.

Project description:Different mating systems have evolved in the fungal kingdom, including a tetrapolar multiallelic mating system in many basidiomycetes. In tetrapolar species, the presence of different alleles at two mating loci (MAT A and MAT B) is necessary for mating to occur. The tetrapolar fungus Serpula lacrymans causes wood-decay in buildings in temperate regions worldwide and is present in Europe with a genetically homogeneous founder population. Using genome sequence data, we annotated the two mating type loci for S. lacrymans and found the expected synteny with other basidiomycetes, except for a retrotransposon being present in one locus (MAT A). We developed markers linked to the MAT A and MAT B regions and used these to investigate the mating type diversity in the European population. Moreover, we found a good match between the genetic markers and functional mating types as revealed by segregation and mating studies. A low diversity of mating types is present in the European S. lacrymans population caused by the founder event where a limited number of genotypes were introduced. This finding contrasts the situation in natural fungal populations where a high diversity of mating types is normally present. Although S. lacrymans has a large and viable population in Europe, we argue that the low mating type diversity restrains the dispersal and establishment of the fungus.

| S-EPMC3564976 | biostudies-literature

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