Nils Högberg

The Plant Cell Wall–Decomposing Machinery Underlies the Functional Diversity of Forest Fungi

Comparative genomic analysis of “dry rot” fungus shows both convergent evolution and divergence among fungal decomposers. Brown rot decay removes cellulose and hemicellulose from wood—residual lignin contributing up to 30% of forest soil carbon—and is derived from an ancestral white rot saprotrophy in which both lignin and cellulose are decomposed. Comparative and functional genomics of the “dry rot” fungus Serpula lacrymans, derived from forest ancestors, demonstrated that the evolution of both ectomycorrhizal biotrophy and brown rot saprotrophy were accompanied by reductions and losses in specific protein families, suggesting adaptation to an intercellular interaction with plant tissue. Transcriptome and proteome analysis also identified differences in wood decomposition in S. lacrymans relative to the brown rot Postia placenta. Furthermore, fungal nutritional mode diversification suggests that the boreal forest biome originated via genetic coevolution of above- and below-ground biota.

Intraspecific genetic variation in Heterobasidion annosum revealed by amplification of minisatellite DNA

DNA from 124 strains of Heterobasidion annosum was amplified using the core sequence of the M13 minisatellite region as primer. The strains were derived from 11 S-, 8 P- and 1 F-intersterility group populations originating in Scandinavia, Germany and Italy. Following electrophoresis the banding patterns of all isolates were compared and 23 fragments were scored. Average band-sharing indices (ABSI) were used to compare genetic diversity within and between populations. Genetic similarity of populations decreased with increasing geographical distance in the S group. In both the S and P intersterility groups, ABSI values were higher within than among populations (70·3 ± 2·3 s.d. and 66·4 ± 2·2, respectively in the S group and 77·0 ± 2·3 and 75·0 ± 2·4, respectively in the P group) indicating local differentiation. The higher values in the P than in the S group indicate that the P group is less variable. ABSI was much lower between S and P group populations (49·2 ± 2·5) than within either group. This result demonstrates the large divergence between these two intersterility groups. In the F population ABSI was higher (68 ± 3·1) than for the comparisons with the S- (50·1 ± 1·6) and P-groups (44·0 ± 2·4). By using discriminant analysis, the agreement between geographical population affiliation and that inferred from banding patterns of amplified DNA was 20·8% within the S group, and 14·9% within the P group. Chi-square test of the discriminant analysis indicated regional differentiation in the S but not in the P intersterility group. The agreement between methods was 98·4% when strains were classified to intersterility group by pairing tests or amplified DNA profiles. Results are consistent with a high degree of exchange between populations of the same intersterility group but low exchange between intersterility groups.

Insight into trade???off between wood decay and parasitism from the genome of a fungal forest pathogen

Parasitism and saprotrophic wood decay are two fungal strategies fundamental for succession and nutrient cycling in forest ecosystems. An opportunity to assess the trade-off between these strategies is provided by the forest pathogen and wood decayer Heterobasidion annosum sensu lato. We report the annotated genome sequence and transcript profiling, as well as the quantitative trait loci mapping, of one member of the species complex: H. irregulare. Quantitative trait loci critical for pathogenicity, and rich in transposable elements, orphan and secreted genes, were identified. A wide range of cellulose-degrading enzymes are expressed during wood decay. By contrast, pathogenic interaction between H. irregulare and pine engages fewer carbohydrate-active enzymes, but involves an increase in pectinolytic enzymes, transcription modules for oxidative stress and secondary metabolite production. Our results show a trade-off in terms of constrained carbohydrate decomposition and membrane transport capacity during interaction with living hosts. Our findings establish that saprotrophic wood decay and necrotrophic parasitism involve two distinct, yet overlapping, processes.

Environmental fluctuations facilitate species co-existence and increase decomposition in communities of wood decay fungi

A fluctuating environment may facilitate co-existence of species, and high species richness may be important for maintaining ecosystem processes under changing environmental conditions. A positive relationship has been found between species richness and primary production in many experiments, and there is now an increasing interest whether similar relationships also apply to microorganisms and decomposition. Basidiomycete fungi are the primary decomposers of wood with the functional groups brown and white rot fungi, which differ with respect to decay strategy. In this study, 16 species of boreal wood decay fungi, 8 brown rot fungi and 8 white rot fungi, were assembled in artificial communities. The aims were to study species persistence, wood decomposition and metabolic efficiency in fungal communities of increasing levels of species richness under constant and fluctuating temperature regimes. Species persistence was generally low, but temperature fluctuations facilitated co-existence of species. Decomposition was highest at intermediate diversity levels under the fluctuating temperature regime. Metabolic efficiency, estimated as the amount of fungal mycelium formed per amount of degraded wood, decreased with increasing community complexity under the fluctuating temperature regime. Brown and white rot fungi differed in decomposition rates and metabolic efficiency, but no synergistic effects were found where the two functional groups were mixed. This study demonstrates how niche differentiation in a variable environment may act to maintain diversity and function. In our experiment, differences in functional responses to the varying temperature rather than resource partitioning between brown and white rot fungi had significant effects. Niche differentiation is likely to be particularly important in maintaining species diversity in communities of wood decaying fungi, which are known from previous studies to be characterised by intense competition, and where otherwise metabolically costly interactions lead to species exclusion and dominance by highly competitive species.

Asian origin and rapid global spread of the destructive dry rot fungus Serpula lacrymans

The dry rot fungus Serpula lacrymans (Basidiomycota) is the most damaging destroyer of wood construction materials in temperate regions. While being a widespread aggressive indoor biodeterioration agent, it is only found in a few natural environments. The geographical source of spread and colonization by this fungus in human environments is thus somewhat of an enigma. Employing genetic markers (amplified fragment length polymorphisms, DNA sequences and microsatellites) on a worldwide sample of specimens, we show that the dry rot fungus is divided into two main lineages; one nonaggressive residing naturally in North America and Asia (var. shastensis), and another aggressive lineage including specimens from all continents, both from natural environments and buildings (var. lacrymans). Our genetic analyses indicate that the two lineages represent well‐differentiated cryptic species. Genetic analyses pinpoint mainland Asia as the origin of the aggressive form var. lacrymans. A few aggressive genotypes have migrated worldwide from Asia to Europe, North and South America and Oceania followed by local population expansions. The very low genetic variation in the founder populations indicate that they have established through recent founder events, for example by infected wood materials transported over land or sea. A separate colonization has happened from mainland Asia to Japan. Our data also indicate that independent immigration events have happened to Oceania from different continents followed by admixture.

Different crop rotation systems as drivers of change in soil bacterial community structure and yield of rice, Oryza sativa

Intensive cropping, especially of rice, is considered to contribute to negative effects not only on soil chemical and biological properties but also on long-term grain yield. Appropriate crop rotation is often practiced as an alternative strategy to overcome the negative side effects of intensive cropping. Although soil microbial diversity and community structure have been shown to respond differently to altered agricultural management practices, little is known about possible links between crop rotation and grain yield on bacterial communities in rice paddy soil. In this study, we investigated the impact of specific rotational crops and compared it with intensive rice cultivation. The main crop rice (Oryza sativa) was rotated with maize (Zea mays) and mungbean (Phaseolus aureus) in different combinations in a system cultivating three crops per year. Soil bacterial communities were studied in two different cropping periods using pyrosequencing of the variable V4 region of the 16S rRNA. Our results showed that rotation with alternative crops increased rice yield by 24–46% depending on rotation structure and that bacterial community structure was altered in the presence of mungbean and/or maize compared to that in rice monoculture. In the crop rotation systems, composition, abundance, and diversity of soil bacterial communities were significantly different and higher than those in rice monoculture. Our results show that effects of crop rotation relate to changes in soil bacterial community structure suggesting that appropriate crop rotations provide a feasible practice to maintain the equilibrium in soil microbial environment for sustainable rice cultivation.

Population genetics of Fomitopsis rosea– a wood‐decay fungus of the old‐growth European taiga

The genetic structure of the wood‐decay fungus Fomitopsis rosea (Alb. et Schw. Fr.) Karst is presented for populations sampled in Russia, Sweden and Finland. A total of 11 variable arbitrary primed (AP)–PCR markers were found to be segregated in a 1:1 ratio. The genotype for each fruiting body was inferred from the genotypes of the haploid single‐spore isolates. Observed heterozygosity was lowest in southern Fennoscandia, the area with the longest history of forestry management. Overall, there was a deficit of heterozygotes compared with frequencies of heterozygotes predicted from Hardy–Weinberg expectations. When we partitioned the deficit of heterozygotes into the hierarchical genetic structure by means of F‐statistics we found that the possible causes for it were both limited gene flow between regions and local nonrandom mating within all populations. Future management for the conservation of F. rosea populations and how the results relate to the life cycle of basidomycete fungi are discussed.

POPULATION STRUCTURE OF THE WOOD DECAY FUNGUS FOMITOPSIS PINICOLA

Three populations of the wood decay fungus Fomitopsis pinicola, one from each of three countries (Sweden, Russia and Lithuania), were studied by means of arbitrary primed PCR. The genetic structure of the populations was assessed by inferring the genotype of the genets by studying the haplotypes of several single-spore isolates from one sporocarp for each individual. Heterozygotes could therefore be detected with a dominant genetic marker. The amplified band and the null allele of all loci segregated in a way that was in agreement with a 50:50 ratio. Genetic analysis showed that the total population as well as the subpopulations had heterozygote frequencies in agreement with Hardy–Weinberg expectations. No population differentiation was detected in spite of large geographical distances among the populations studied. We also compared the methods of somatic incompatibility and AP-PCR in terms of their value in detecting fungal genets. This was tested for a sample of dikaryotic mycelia from Switzerland. For the tested material the two methods gave congruent results.

Extremely low AFLP variation in the European dry rot fungus ( Serpula lacrymans ): implications for self/nonself-recognition

The devastating dry rot fungus, Serpula lacrymans, has a worldwide occurrence in buildings. We investigated the genetic variation in European isolates belonging to five vegetative compatibility groups (VCGs) by AFLP analysis. Our results indicate that S. lacrymans in Europe is genetically extremely homogenous; only five out of 308 scored AFLP fragments (1.6 %) were polymorphic. In contrast, S. himantioides, the closest relative of S. lacrymans, possessed 31.3 % polymorphic fragments (84 out of 268). AFLP polymorphisms observed in S. lacrymans were distributed independently of the VCG boundaries, indicating that the VCGs do not represent clones but that different genets of S. lacrymans frequently share similar vic alleles due to low genetic variation. Thus, although the European S. lacrymans is genetically extremely homogeneous, and our results suggest that the species reproduces and spreads mainly sexually and not by clones.

Genotypic diversity and migration patterns of Phytophthora infestans in the Nordic countries.

In this study we investigated the genotypic diversity and the migration patterns of Phytophthora infestans in the Nordic countries. Isolates of P. infestans from outbreaks in 43 fields sampled in 2008 were collected using stratified sampling with country, field, and disease foci as the different strata. Microsatellites were used as markers to determine the genotypic variation in the sampled material. The results show a high genotypic variation of P. infestans in the Nordic countries with most of the genotypes found only once among the collected isolates. The major part of the genotypic variation was observed within the fields, with low differentiation between the fields. The observed low association of alleles among loci is consistent with frequent sexual reproduction of P. infestans in the Nordic countries. Coalescence analyses did not support a single common population for the four countries, thus indicating some degree of geographic differentiation. The analyses of migration patterns showed differing levels of gene flow among the Nordic countries. No correlation between migration rates and geographical distance could be seen. This could be explained by different degrees of genetic similarity between the pathogen populations in the different countries.