Publications by authors named "Duur Aanen"

61 Publications

Evolution: Ant trail pheromones promote ant-aphid mutualisms.

Curr Biol 2021 Nov;31(21):R1437-R1439

Department of Plant Sciences, Laboratory of Genetics, Wageningen University, 6708 PB Wageningen, The Netherlands.

A new study shows that trail pheromones produced by an invasive ant species suppress the dispersal and stimulate the reproduction of cotton aphids that the ants can 'milk' for honeydew. Aphids use these pheromones as a signal of ant presence and respond adaptively, analogous to early stages of animal husbandry where animals were attracted to human settlements.
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http://dx.doi.org/10.1016/j.cub.2021.09.046DOI Listing
November 2021

Phylogenetic and phylogenomic analyses reveal two new genera and three new species of ophiostomatalean fungi from termite fungus combs.

Mycologia 2021 Nov-Dec;113(6):1199-1217. Epub 2021 Sep 3.

Department of Biochemistry, Genetics and Microbiology, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Private Bag X20, Pretoria, 0028 South Africa.

The Ophiostomatales (Ascomycota) accommodates more than 300 species characterized by similar morphological adaptations to arthropod dispersal. Most species in this order are wood-inhabiting fungi associated with bark or ambrosia beetles. However, a smaller group of species occur in other niches such as in soil and infructescences. Recent surveys of fungus gardens (fungus combs) of fungus-growing termites led to the discovery of characteristic ophiostomatalean-like fruiting structures. In this study, these ophiostomatalean-like fungi were identified using morphological characteristics, conventional molecular markers, and whole genome sequencing. In addition, the influence of the extracts derived from various parts of combs on the growth of these fungi in culture was considered. Based on phylogenomic analyses, two new genera ( and ) were introduced to accommodate these ophiostomatalean species. Phylogenetic analyses revealed that the isolates resided in three well-supported lineages, and these were described as three new species (, and ). Culture-based studies showed that these species do not depend on the comb material for growth.
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http://dx.doi.org/10.1080/00275514.2021.1950455DOI Listing
September 2021

Ancestral predisposition toward a domesticated lifestyle in the termite-cultivated fungus Termitomyces.

Curr Biol 2021 Oct 16;31(19):4413-4421.e5. Epub 2021 Aug 16.

Laboratory of Genetics, Wageningen University & Research, Droevendaalsesteeg 1, 6708PB Wageningen, the Netherlands. Electronic address:

The ancestor of termites relied on gut symbionts for degradation of plant material, an association that persists in all termite families. However, the single-lineage Macrotermitinae has additionally acquired a fungal symbiont that complements digestion of food outside the termite gut. Phylogenetic analysis has shown that fungi grown by these termites form a clade-the genus Termitomyces-but the events leading toward domestication remain unclear. To address this, we reconstructed the lifestyle of the common ancestor of Termitomyces using a combination of ecological data with a phylogenomic analysis of 21 related non-domesticated species and 25 species of Termitomyces. We show that the closely related genera Blastosporella and Arthromyces also contain insect-associated species. Furthermore, the genus Arthromyces produces asexual spores on the mycelium, which may facilitate insect dispersal when growing on aggregated subterranean fecal pellets of a plant-feeding insect. The sister-group relationship between Arthromyces and Termitomyces implies that insect association and asexual sporulation, present in both genera, preceded the domestication of Termitomyces and did not follow domestication as has been proposed previously. Specialization of the common ancestor of these two genera on an insect-fecal substrate is further supported by similar carbohydrate-degrading profiles between Arthromyces and Termitomyces. We describe a set of traits that may have predisposed the ancestor of Termitomyces toward domestication, with each trait found scattered in related taxa outside of the termite-domesticated clade. This pattern indicates that the origin of the termite-fungus symbiosis may not have required large-scale changes of the fungal partner.
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http://dx.doi.org/10.1016/j.cub.2021.07.070DOI Listing
October 2021

Cytoplasmic Mixing, Not Nuclear Coexistence, Can Explain Somatic Incompatibility in Basidiomycetes.

Microorganisms 2021 Jun 8;9(6). Epub 2021 Jun 8.

Laboratory of Genetics, Wageningen University and Research, 6708 PB Wageningen, The Netherlands.

Nonself recognition leading to somatic incompatibility (SI) is commonly used by mycologists to distinguish fungal individuals. Despite this, the process remains poorly understood in basidiomycetes as all current models of SI are based on genetic and molecular research in ascomycete fungi. Ascomycete fungi are mainly found in a monokaryotic stage, with a single type of haploid nuclei, and only briefly during mating do two genomes coexist in heterokaryotic cells. The sister phylum, Basidiomycota, differs in several relevant aspects. Basidiomycete fungi have an extended heterokaryotic stage, and SI is generally observed between heterokaryons instead of between homokaryons. Additionally, considerable nuclear migration occurs during a basidiomycete mating reaction, introducing a nucleus into a resident homokaryon with cytoplasmic mixing limited to the fused or neighboring cells. To accommodate these differences, we describe a basidiomycete model for nonself recognition using post-translational modification, based on a reader-writer system as found in other organisms. This post-translational modification combined with nuclear migration allows for the coexistence of two genomes in one individual while maintaining nonself recognition during all life stages. Somewhat surprisingly, this model predicts localized cell death during mating, which is consistent with previous observations but differs from the general assumptions of basidiomycete mating. This model will help guide future research into the mechanisms behind basidiomycete nonself recognition.
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http://dx.doi.org/10.3390/microorganisms9061248DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8229728PMC
June 2021

Genome reduction and relaxed selection is associated with the transition to symbiosis in the basidiomycete genus .

iScience 2021 Jun 1;24(6):102680. Epub 2021 Jun 1.

Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen Ø, Denmark.

Insights into the genomic consequences of symbiosis for basidiomycete fungi associated with social insects remain sparse. Capitalizing on viability of spores from centuries-old herbarium specimens of free-living, facultative, and specialist termite-associated fungi, we obtained genomes of 10 specimens, including two type species described by Linnaeus >240 years ago. We document that the transition to termite association was accompanied by significant reductions in genome size and gene content, accelerated evolution in protein-coding genes, and reduced functional capacities for oxidative stress responses and lignin degradation. Functional testing confirmed that termite specialists perform worse under oxidative stress, while all lineages retained some capacity to cleave lignin. Mitochondrial genomes of termite associates were significantly larger; possibly driven by smaller population sizes or reduced competition, supported by apparent loss of certain biosynthetic gene clusters. Our findings point to relaxed selection that mirrors genome traits observed among obligate endosymbiotic bacteria of many insects.
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http://dx.doi.org/10.1016/j.isci.2021.102680DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8220239PMC
June 2021

Somatic deficiency causes reproductive parasitism in a fungus.

Nat Commun 2021 02 4;12(1):783. Epub 2021 Feb 4.

Laboratory of Genetics, Wageningen University, Wageningen, The Netherlands.

Some multicellular organisms can fuse because mergers potentially provide mutual benefits. However, experimental evolution in the fungus Neurospora crassa has demonstrated that free fusion of mycelia favours cheater lineages, but the mechanism and evolutionary dynamics of this exploitation are unknown. Here we show, paradoxically, that all convergently evolved cheater lineages have similar fusion deficiencies. These mutants are unable to initiate fusion but retain access to wild-type mycelia that fuse with them. This asymmetry reduces cheater-mutant contributions to somatic substrate-bound hyphal networks, but increases representation of their nuclei in the aerial reproductive hyphae. Cheaters only benefit when relatively rare and likely impose genetic load reminiscent of germline senescence. We show that the consequences of somatic fusion can be unequally distributed among fusion partners, with the passive non-fusing partner profiting more. We discuss how our findings may relate to the extensive variation in fusion frequency of fungi found in nature.
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http://dx.doi.org/10.1038/s41467-021-21050-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7862218PMC
February 2021

The Longevity of Colonies of Fungus-Growing Termites and the Stability of the Symbiosis.

Insects 2020 Aug 13;11(8). Epub 2020 Aug 13.

Laboratory of Genetics, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands.

The agricultural mutualistic symbiosis between macrotermitine termites and fungi is obligate for both partners. The termites provide a protective growth environment for the fungus by cultivating it inside their colony and providing it with foraged plant material. The termites use the fungus for plant substrate degradation, and the production of asexual fruiting bodies for nourishment and re-inoculation of the fungus garden. The termite colony can reach an age of up to several decades, during which time it is believed that a single fungal monoculture is asexually propagated by the offspring of a single founding royal pair. The termite-fungus mutualism has a long evolutionary history dating back more than 30 million years. Both on the time-scale of a termite colony lifespan and that of the mutualistic symbiosis, questions arise about stability. We address the physical stability of the mound, the termite colony and the monoculture fungal garden during a colony's lifetime. On the long-term evolutionary scale, we address the stability of the symbiosis, where horizontal transmission of the symbiotic fungus raises the question of how the mutualistic interaction between host and symbiont persists over generations.
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http://dx.doi.org/10.3390/insects11080527DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7469218PMC
August 2020

Asexual and sexual reproduction are two separate developmental pathways in a species.

Biol Lett 2020 08 12;16(8):20200394. Epub 2020 Aug 12.

Department of Plant Sciences, Laboratory of Genetics, Wageningen University, Wageningen, The Netherlands.

Although mutualistic symbioses per definition are beneficial for interacting species, conflict may arise if partners reproduce independently. We address how this reproductive conflict is regulated in the obligate mutualistic symbiosis between fungus-growing termites and fungi. Even though the termites and their fungal symbiont disperse independently to establish new colonies, dispersal is correlated in time. The fungal symbiont typically forms mushrooms a few weeks after the colony has produced dispersing alates. It is thought that this timing is due to a trade-off between alate and worker production; alate production reduces resources available for worker production. As workers consume the fungus, reduced numbers of workers will allow mushrooms to 'escape' from the host colony. Here, we test a specific version of this hypothesis: the typical asexual structures found in all species of -nodules-are immature stages of mushrooms that are normally harvested by the termites at a primordial stage. We refute this hypothesis by showing that nodules and mushroom primordia are macro- and microscopically different structures and by showing that in the absence of workers, primordia do, and nodules do not grow out into mushrooms. It remains to be tested whether termite control of primordia formation or of primordia outgrowth mitigates the reproductive conflict.
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http://dx.doi.org/10.1098/rsbl.2020.0394DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7480157PMC
August 2020

Germline Evolution: Sequestered Cells or Immortal Strands?

Authors:
Duur K Aanen

Curr Biol 2019 08;29(16):R799-R801

Department of Plant Sciences, Laboratory of Genetics, Wageningen University, 6708 PB Wageningen, Netherlands. Electronic address:

Mutation accumulation in long-lived fairy-ring mushrooms is orders of magnitude lower than predicted based on per-cell division mutation rates in other organisms. A possible explanation is the maintenance of 'immortal' template-DNA in the active periphery of the fairy ring.
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http://dx.doi.org/10.1016/j.cub.2019.07.033DOI Listing
August 2019

Disease-free monoculture farming by fungus-growing termites.

Sci Rep 2019 06 19;9(1):8819. Epub 2019 Jun 19.

Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, Building 3, 2100, Copenhagen East, Denmark.

Fungus-growing termites engage in an obligate mutualistic relationship with Termitomyces fungi, which they maintain in monocultures on specialised fungus comb structures, without apparent problems with infectious diseases. While other fungi have been reported in the symbiosis, detailed comb fungal community analyses have been lacking. Here we use culture-dependent and -independent methods to characterise fungus comb mycobiotas from three fungus-growing termite species (two genera). Internal Transcribed Spacer (ITS) gene analyses using 454 pyrosequencing and Illumina MiSeq showed that non-Termitomyces fungi were essentially absent in fungus combs, and that Termitomyces fungal crops are maintained in monocultures as heterokaryons with two or three abundant ITS variants in a single fungal strain. To explore whether the essential absence of other fungi within fungus combs is potentially due to the production of antifungal metabolites by Termitomyces or comb bacteria, we performed in vitro assays and found that both Termitomyces and chemical extracts of fungus comb material can inhibit potential fungal antagonists. Chemical analyses of fungus comb material point to a highly complex metabolome, including compounds with the potential to play roles in mediating these contaminant-free farming conditions in the termite symbiosis.
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http://dx.doi.org/10.1038/s41598-019-45364-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6584615PMC
June 2019

Enrichment of G4DNA and a Large Inverted Repeat Coincide in the Mitochondrial Genomes of Termitomyces.

Genome Biol Evol 2019 07;11(7):1857-1869

Laboratory of Genetics, Wageningen University & Research, The Netherlands.

Mitochondria retain their own genome, a hallmark of their bacterial ancestry. Mitochondrial genomes (mtDNA) are highly diverse in size, shape, and structure, despite their conserved function across most eukaryotes. Exploring extreme cases of mtDNA architecture can yield important information on fundamental aspects of genome biology. We discovered that the mitochondrial genomes of a basidiomycete fungus (Termitomyces spp.) contain an inverted repeat (IR), a duplicated region half the size of the complete genome. In addition, we found an abundance of sequences capable of forming G-quadruplexes (G4DNA); structures that can disrupt the double helical formation of DNA. G4DNA is implicated in replication fork stalling, double-stranded breaks, altered gene expression, recombination, and other effects. To determine whether this occurrence of IR and G4DNA was correlated within the genus Termitomyces, we reconstructed the mitochondrial genomes of 11 additional species including representatives of several closely related genera. We show that the mtDNA of all sampled species of Termitomyces and its sister group, represented by the species Tephrocybe rancida and Blastosporella zonata, are characterized by a large IR and enrichment of G4DNA. To determine whether high mitochondrial G4DNA content is common in fungi, we conducted the first broad survey of G4DNA content in fungal mtDNA, revealing it to be a highly variable trait. The results of this study provide important direction for future research on the function and evolution of G4DNA and organellar IRs.
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http://dx.doi.org/10.1093/gbe/evz122DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6609731PMC
July 2019

Mutation-rate plasticity and the germline of unicellular organisms.

Proc Biol Sci 2019 05;286(1902):20190128

Department of Plant Sciences, Laboratory of Genetics, Wageningen University , 6708 PB Wageningen , The Netherlands.

The mutation rate is a fundamental factor in evolutionary genetics. Recently, mutation rates were found to be strongly reduced at high density in a wide range of unicellular organisms, prokaryotic and eukaryotic. Independently, cell division was found to become more asymmetrical at increasing density in diverse organisms; some 'mother' cells continue dividing, while their 'offspring' cells do not divide further. Here, we investigate how this increased asymmetry in cell division at high density can be reconciled with reduced mutation-rate estimates. We calculated the expected number of mutant cells due to replication errors under various modes of segregation of template-DNA strands and copy-DNA strands, both under symmetrical (exponential) and asymmetrical (linear) growth. We show that the observed reduction in the mutation rate at high density can be explained if mother cells preferentially retain the template-DNA strands, since new mutations are then confined to non-dividing daughter cells, thus reducing the spread of mutant cells. Any other inheritance mode results in an increase in the number of mutant cells at higher density. The proposed hypothesis that patterns of DNA-strand segregation are density-dependent fundamentally challenges our current understanding of mutation-rate estimates and extends the distinction between germline and soma to unicellular organisms.
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http://dx.doi.org/10.1098/rspb.2019.0128DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6532511PMC
May 2019

Reviewing the taxonomy of Podaxis: Opportunities for understanding extreme fungal lifestyles.

Fungal Biol 2019 03 11;123(3):183-187. Epub 2019 Jan 11.

Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

There are few environments more hostile and species-poor than deserts and the mounds of Nasutitermitinae termites. However, despite the very different adaptations required to survive in such extreme and different environments, the fungal genus Podaxis is capable of surviving in both: where few other fungi are reported to grow. Despite their prominence in the landscape and their frequent documentation by early explorers, there has been relatively little research into the genus. Originally described by Linnaeus in 1771, in the early 20th Century, the then ∼25 species of Podaxis were almost entirely reduced into one species: Podaxis pistillaris. Since this reduction, several new species of Podaxis have been described but without consideration of older descriptions. This has resulted in 44 recognised species names in Index Fungorum but the vast majority of studies and fungarium specimens still refer to P. pistillaris. Studies of Podaxis' extremely different lifestyles is hampered by its effective reduction to a single-species genus. Here we examine the history of the taxonomy of Podaxis before focusing on its extreme lifestyles. From this, we consider how the muddled taxonomy of Podaxis may be resolved; opening up further avenues for future research into this enigmatic fungal genus.
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http://dx.doi.org/10.1016/j.funbio.2019.01.001DOI Listing
March 2019

Nuclear arms races: Experimental evolution for mating success in the mushroom-forming fungus Schizophyllum commune.

PLoS One 2018 27;13(12):e0209671. Epub 2018 Dec 27.

Laboratory of Genetics, Wageningen University, Wageningen, The Netherlands.

When many gametes compete to fertilize a limited number of compatible gametes, sexual selection will favour traits that increase competitive success during mating. In animals and plants, sperm and pollen competition have yielded many interesting adaptations for improved mating success. In fungi, similar processes have not been shown directly yet. We test the hypothesis that sexual selection can increase competitive fitness during mating, using experimental evolution in the mushroom-forming fungus Schizophyllum commune (Basidiomycota). Mating in mushroom fungi occurs by donation of nuclei to a mycelium. These fertilizing 'male' nuclei migrate through the receiving 'female' mycelium. In our setup, an evolving population of nuclei was serially mated with a non-evolving female mycelium for 20 sexual generations. From the twelve tested evolved lines, four had increased and one had decreased fitness relative to an unevolved competitor. Even though only two of those five remained significant after correcting for multiple comparisons, for all five lines we found a correlation between the efficiency with which the female mycelium is accessed and fitness, providing additional circumstantial evidence for fitness change in those five lines. In two lines, fitness change was also accompanied by increased spore production. The one line with net reduced competitive fitness had increased spore production, but reduced fertilisation efficiency. We did not find trade-offs between male reproductive success and other fitness components. We compare these findings with examples of sperm and pollen competition and show that many similarities between these systems and nuclear competition in mushrooms exist.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0209671PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6320016PMC
May 2019

The obligate alkalophilic soda-lake fungus Sodiomyces alkalinus has shifted to a protein diet.

Mol Ecol 2018 12 22;27(23):4808-4819. Epub 2018 Nov 22.

Laboratory of Genetics, Wageningen University, Wageningen, The Netherlands.

Sodiomyces alkalinus is one of the very few alkalophilic fungi, adapted to grow optimally at high pH. It is widely distributed at the plant-deprived edges of extremely alkaline lakes and locally abundant. We sequenced the genome of S. alkalinus and reconstructed evolution of catabolic enzymes, using a phylogenomic comparison. We found that the genome of S. alkalinus is larger, but its predicted proteome is smaller and heavily depleted of both plant-degrading enzymes and proteinases, when compared to its closest plant-pathogenic relatives. Interestingly, despite overall losses, S. alkalinus has retained many proteinases families and acquired bacterial cell wall-degrading enzymes, some of them via horizontal gene transfer from bacteria. This fungus has very potent proteolytic activity at high pH values, but slowly induced low activity of cellulases and hemicellulases. Our experimental and in silico data suggest that plant biomass, a common food source for most fungi, is not a preferred substrate for S. alkalinus in its natural environment. We conclude that the fungus has abandoned the ancestral plant-based diet and has become specialized in a more protein-rich food, abundantly available in soda lakes in the form of prokaryotes and small crustaceans.
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http://dx.doi.org/10.1111/mec.14912DOI Listing
December 2018

The disposable male- the ultimate emancipation of females?

Authors:
Duur K Aanen

BMC Biol 2018 09 25;16(1):106. Epub 2018 Sep 25.

Department of Plant Sciences, Laboratory of Genetics, Wageningen University, 6708 PB Wageningen, Wageningen, The Netherlands.

Sexual reproduction is costly compared to asexual reproduction, in particular because males generally contribute little to offspring. Research published today in BMC Biology shows that some populations of a termite species have disposed of males altogether. However, this need not necessarily be seen as a victory for the females, since males in most termite societies are active colony members that contribute their fair share to colony tasks.
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http://dx.doi.org/10.1186/s12915-018-0574-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6154933PMC
September 2018

Phylogeny of Paecilomyces, the causal agent of pistachio and some other trees dieback disease in Iran.

PLoS One 2018 24;13(7):e0200794. Epub 2018 Jul 24.

Laboratory of Genetics, Plant Sciences Department, Healthy Food and Living Environment Faculty, Wageningen University, Wageningen, The Netherlands.

One of the most important fungal agents of pistachio dieback disease belongs to the ascomycete genus Paecilomyces that has been identified as P. variotii. In 2012-2014, 700 plant samples from pistachio trees and 27 other plant species with dieback symptoms were collected from 10 provinces of Iran. Of the 567 pistachio samples, 277 Paecilomyces strains were obtained and from the 133 samples of other plants (except pistachio and including Pistacia mutica, Punica granatum, Prunus amygdalus, Caesalpinia gilliesii, Nerium oleander, Tamarix aphylla, Tamarix hispida and Haloxylon sp.), 23 fungal isolates were recovered and five isolates were obtained from the air of infected pistachio orchards. Based on morphology, all 305 isolates were identified as P. variotii. Physiological studies revealed that 299 isolates belong to P. formosus. Three isolates were assigned to P. variotii, while three isolates could not be assigned to any of the known species. Of the 305 isolates, 62 were selected for phylogenetic analysis based on DNA variation (ITS, β-tubulin and calmodulin). This analysis showed that all of our isolates form a clade with P. formosus. P. formosus consists of the three former species P. formosa, P. lecythidis and P. maximus. This study shows that our isolates form a strongly supported clade with strains of P. lecythidis. So, the causal agent of dieback disease of pistachio and other examined trees is P. formosus which is closely related to the former species P. lecythidis and has some differences with the former species P. formosa and P. maximus. Based on phylogenetic studies P. formosus thus seems to be a species complex that could be divided into three separate species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0200794PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6057626PMC
January 2019

Social Immunity: The Disposable Individual.

Authors:
Duur K Aanen

Curr Biol 2018 04;28(7):R322-R324

Department of Plant Sciences, Laboratory of Genetics, Wageningen University, 6708 PB Wageningen, Netherlands. Electronic address:

Workers in an ant colony can kill fungus-infected brood, thereby protecting the rest of the colony from fungal infection. This form of social immunity is analogous to the immune system of multicellular organisms where immune cells kill infected cells.
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http://dx.doi.org/10.1016/j.cub.2018.02.050DOI Listing
April 2018

Enzyme Activities at Different Stages of Plant Biomass Decomposition in Three Species of Fungus-Growing Termites.

Appl Environ Microbiol 2018 03 14;84(5). Epub 2018 Feb 14.

Centre for Social Evolution, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

Fungus-growing termites rely on mutualistic fungi of the genus and gut microbes for plant biomass degradation. Due to a certain degree of symbiont complementarity, this tripartite symbiosis has evolved as a complex bioreactor, enabling decomposition of nearly any plant polymer, likely contributing to the success of the termites as one of the main plant decomposers in the Old World. In this study, we evaluated which plant polymers are decomposed and which enzymes are active during the decomposition process in two major genera of fungus-growing termites. We found a diversity of active enzymes at different stages of decomposition and a consistent decrease in plant components during the decomposition process. Furthermore, our findings are consistent with the hypothesis that termites transport enzymes from the older mature parts of the fungus comb through young worker guts to freshly inoculated plant substrate. However, preliminary fungal RNA sequencing (RNA-seq) analyses suggest that this likely transport is supplemented with enzymes produced Our findings support that the maintenance of an external fungus comb, inoculated with an optimal mixture of plant material, fungal spores, and enzymes, is likely the key to the extraordinarily efficient plant decomposition in fungus-growing termites. Fungus-growing termites have a substantial ecological footprint in the Old World (sub)tropics due to their ability to decompose dead plant material. Through the establishment of an elaborate plant biomass inoculation strategy and through fungal and bacterial enzyme contributions, this farming symbiosis has become an efficient and versatile aerobic bioreactor for plant substrate conversion. Since little is known about what enzymes are expressed and where they are active at different stages of the decomposition process, we used enzyme assays, transcriptomics, and plant content measurements to shed light on how this decomposition of plant substrate is so effectively accomplished.
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http://dx.doi.org/10.1128/AEM.01815-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5812949PMC
March 2018

Symbiogenesis: Beyond the endosymbiosis theory?

J Theor Biol 2017 12 18;434:99-103. Epub 2017 Aug 18.

Life Sciences Department, The Natural History Museum, London SW7 5BD, UK.

Symbiogenesis, literally 'becoming by living together', refers to the crucial role of symbiosis in major evolutionary innovations. The term usually is reserved for the major transition to eukaryotes and to photosynthesising eukaryotic algae and plants by endosymbiosis. However, in some eukaryote lineages endosymbionts have been lost secondarily, showing that symbiosis can trigger a major evolutionary innovation, even if symbionts were lost secondarily. This leads to the intriguing possibility that symbiosis has played a role in other major evolutionary innovations as well, even if not all extant representatives of such groups still have the symbiotic association. We evaluate this hypothesis for two innovations in termites (Termitoidae, also known informally as "Isoptera"): i) the role of flagellate gut protist symbionts in the transition to eusociality from cockroach-like ancestors, and ii) the role of non-gut associated symbionts in the transition to 'higher' termites, characterized by the absence of flagellate gut protists. In both cases we identify a crucial role for symbionts, even though in both cases, subsequently, symbionts were lost again in some lineages. We also briefly discuss additional possible examples of symbiogenesis. We conclude that symbiogenesis is more broadly applicable than just for the endosymbiotic origin of eukaryotes and photosynthetic eukaryotes, and may be a useful concept to acknowledge the important role of symbiosis for evolutionary innovation. However, we do not accept Lynn Margulis's view that symbiogenesis will lead to a paradigm shift from neoDarwinism, as the role of symbiosis in evolutionary change can be integrated with existing theory perfectly.
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http://dx.doi.org/10.1016/j.jtbi.2017.08.001DOI Listing
December 2017

Weird sex: the underappreciated diversity of sexual reproduction.

Philos Trans R Soc Lond B Biol Sci 2016 Oct;371(1706)

Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland.

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http://dx.doi.org/10.1098/rstb.2016.0262DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5031627PMC
October 2016

Unholy marriages and eternal triangles: how competition in the mushroom life cycle can lead to genomic conflict.

Philos Trans R Soc Lond B Biol Sci 2016 10;371(1706)

Laboratory of Genetics, Plant Sciences Group, Wageningen University, 6700 AA Wageningen, The Netherlands

In the vast majority of sexual life cycles, fusion between single-celled gametes is directly followed by nuclear fusion, leading to a diploid zygote and a lifelong commitment between two haploid genomes. Mushroom-forming basidiomycetes differ in two key respects. First, the multicellular haploid mating partners are fertilized in their entirety, each cell being a gamete that simultaneously can behave as a female, i.e. contributing the cytoplasm to a zygote by accepting nuclei, and a male gamete, i.e. only donating nuclei to the zygote. Second, after gamete union, the two haploid genomes remain separate so that the main vegetative stage, the dikaryon, has two haploid nuclei per cell. Only when the dikaryon produces mushrooms, do the nuclei fuse to enter a short diploid stage, immediately followed by meiosis and haploid spore formation. So in basidiomycetes, gamete fusion and genome mixing (sex) are separated in time. The 'living apart together' of nuclei in the dikaryon maintains some autonomy for nuclei to engage in a relationship with a different nucleus. We show that competition among the two nuclei of the dikaryon for such 'extramarital affairs' may lead to genomic conflict by favouring genes beneficial at the level of the nucleus, but deleterious at that of the dikaryon.This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'.
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http://dx.doi.org/10.1098/rstb.2015.0533DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5031618PMC
October 2016

Phylogenetic analyses of Podaxis specimens from Southern Africa reveal hidden diversity and new insights into associations with termites.

Fungal Biol 2016 09 7;120(9):1065-76. Epub 2016 Jun 7.

Centre for Social Evolution, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Denmark. Electronic address:

Although frequently found on mounds of the grass-cutting termite genus Trinervitermes, virtually nothing is known about the natural history of the fungal genus Podaxis (Agaricaceae) nor why it associates with termite mounds. More than 40 species of this secotioid genus have been described since Linnaeus characterised the first species in 1771. However, taxonomic confusion arose when most of these species were reduced to synonymy with Podaxis pistillaris in 1933. Although a few more species have since been described, the vast majority of specimens worldwide are still treated as P. pistillaris. Using 45 fresh and herbarium specimens from Southern Africa, four from North America and one each from Ethiopia, and Kenya, we constructed the first comprehensive phylogeny of the genus. Four of the genotyped specimens were more than 100 y old. With the exception of the type specimen of Podaxis rugospora, all herbarium specimens were labelled as P. pistillaris or Podaxis sp. However, our data shows that the genus contains at least five well-supported clades with significant inter-clade differences in spore length, width and wall thickness, and fruiting body length, supporting that clades likely represent distinct Podaxis species. Certain clades consistently associate with termites while others appear entirely free-living.
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http://dx.doi.org/10.1016/j.funbio.2016.05.011DOI Listing
September 2016

Pseudoxylallemycins A-F, Cyclic Tetrapeptides with Rare Allenyl Modifications Isolated from Pseudoxylaria sp. X802: A Competitor of Fungus-Growing Termite Cultivars.

Org Lett 2016 07 24;18(14):3338-41. Epub 2016 Jun 24.

Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute , Beutenbergstraße 11a, 07745 Jena, Germany.

Based on fungus-fungus pairing assays and HRMS-based dereplication strategy, six new cyclic tetrapeptides, pseudoxylallemycins A-F (1-6), were isolated from the termite-associated fungus Pseudoxylaria sp. X802. Structures were characterized using NMR spectroscopy, HRMS, and Marfey's reaction. Pseudoxylallemycins B-D (2-4) possess a rare and chemically accessible allene moiety amenable for synthetic modifications, and derivatives A-D showed antimicrobial activity against Gram-negative human-pathogenic Pseudomonas aeruginosa and antiproliferative activity against human umbilical vein endothelial cells and K-562 cell lines.
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http://dx.doi.org/10.1021/acs.orglett.6b01437DOI Listing
July 2016

Oligocene Termite Nests with In Situ Fungus Gardens from the Rukwa Rift Basin, Tanzania, Support a Paleogene African Origin for Insect Agriculture.

PLoS One 2016 22;11(6):e0156847. Epub 2016 Jun 22.

Department of Biomedical Sciences, Heritage College of Osteopathic Medicine, Ohio University, Athens, Ohio, 45701, United States of America.

Based on molecular dating, the origin of insect agriculture is hypothesized to have taken place independently in three clades of fungus-farming insects: the termites, ants or ambrosia beetles during the Paleogene (66-24 Ma). Yet, definitive fossil evidence of fungus-growing behavior has been elusive, with no unequivocal records prior to the late Miocene (7-10 Ma). Here we report fossil evidence of insect agriculture in the form of fossil fungus gardens, preserved within 25 Ma termite nests from southwestern Tanzania. Using these well-dated fossil fungus gardens, we have recalibrated molecular divergence estimates for the origins of termite agriculture to around 31 Ma, lending support to hypotheses suggesting an African Paleogene origin for termite-fungus symbiosis; perhaps coinciding with rift initiation and changes in the African landscape.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0156847PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4917219PMC
July 2017

Experimental evolution reveals that high relatedness protects multicellular cooperation from cheaters.

Nat Commun 2016 May 3;7:11435. Epub 2016 May 3.

Department of Plant Sciences, Laboratory of Genetics, Wageningen University, Wageningen 6708 PB, The Netherlands.

In multicellular organisms, there is a potential risk that cheating mutants gain access to the germline. Development from a single-celled zygote resets relatedness among cells to its maximum value each generation, which should accomplish segregation of cheating mutants from non-cheaters and thereby protect multicellular cooperation. Here we provide the crucial direct comparison between high- and low-relatedness conditions to test this hypothesis. We allow two variants of the fungus Neurospora crassa to evolve, one with and one without the ability to form chimeras with other individuals, thus generating two relatedness levels. While multicellular cooperation remains high in the high-relatedness lines, it significantly decreases in all replicate low-relatedness lines, resulting in an average threefold decrease in spore yield. This reduction is caused by cheating mutants with reduced investment in somatic functions, but increased competitive success when fusing with non-cheaters. Our experiments demonstrate that high genetic relatedness is crucial to sustain multicellular cooperation.
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http://dx.doi.org/10.1038/ncomms11435DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4857390PMC
May 2016

Entomology: A Bee Farming a Fungus.

Curr Biol 2015 Nov;25(22):R1072-4

Laboratory of Genetics, Wageningen University, PO Boz 309, 6700 AH Wageningen, The Netherlands.

Farming is done not only by humans, but also by some ant, beetle and termite species. With the discovery of a stingless bee farming a fungus that provides benefits to its larvae, bees can be added to this list.
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http://dx.doi.org/10.1016/j.cub.2015.09.062DOI Listing
November 2015

Experimental demonstration of the benefits of somatic fusion and the consequences for allorecognition.

Evolution 2015 Apr 30;69(4):1091-9. Epub 2015 Mar 30.

Laboratory of Genetics, Wageningen University, Droevendaalsesteeg 1, 6708 PD, Wageningen, The Netherlands.

Allorecognition, the ability to distinguish "self" from "nonself" based on allelic differences at allorecognition loci, is common in all domains of life. Allorecognition restricts the opportunities for social parasitism, and is therefore crucial for the evolution of cooperation. However, the maintenance of allorecognition diversity provides a paradox. If allorecognition is costly relative to cooperation, common alleles will be favored. Thus, the cost of allorecognition may reduce the genetic variation upon which allorecognition crucially relies, a prediction now known as "Crozier's paradox." We establish the relative costs of allorecognition, and their consequences for the short-term evolution of recognition labels theoretically predicted by Crozier. We use fusion among colonies of the fungus Neurospora crassa, regulated by highly variable allorecognition genes, as an experimental model system. We demonstrate that fusion among colonies is mutually beneficial, relative to absence of fusion upon allorecognition. This benefit is due not only to absence of mutual antagonism, which occurs upon allorecognition, but also to an increase in colony size per se. We then experimentally demonstrate that the benefit of fusion selects against allorecognition diversity, as predicted by Crozier. We discuss what maintains allorecognition diversity.
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http://dx.doi.org/10.1111/evo.12626DOI Listing
April 2015

Developmental Biology. How a long-lived fungus keeps mutations in check.

Authors:
Duur K Aanen

Science 2014 Nov 20;346(6212):922-3. Epub 2014 Nov 20.

Department of Plant Sciences, Laboratory of Genetics, Wageningen University, 6708 PB Wageningen, Netherlands.

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http://dx.doi.org/10.1126/science.1261401DOI Listing
November 2014

Selection against somatic parasitism can maintain allorecognition in fungi.

Fungal Genet Biol 2014 Dec 8;73:128-37. Epub 2014 Oct 8.

Laboratory of Genetics, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands. Electronic address:

Fusion between multicellular individuals is possible in many organisms with modular, indeterminate growth, such as marine invertebrates and fungi. Although fusion may provide various benefits, fusion usually is restricted to close relatives by allorecognition, also called heterokaryon or somatic incompatibility in fungi. A possible selective explanation for allorecognition is protection against somatic parasites. Such mutants contribute less to colony functions but more to reproduction. However, previous models testing this idea have failed to explain the high diversity of allorecognition alleles in nature. These models did not, however, consider the possible role of spatial structure. We model the joint evolution of allorecognition and somatic parasitism in a multicellular organism resembling an asexual ascomycete fungus in a spatially explicit simulation. In a 1000-by-1000 grid, neighbouring individuals can fuse, but only if they have the same allotype. Fusion with a parasitic individual decreases the total reproductive output of the fused individuals, but the parasite compensates for this individual-level fitness reduction by a disproportional share of the offspring. Allorecognition prevents the invasion of somatic parasites, and vice versa, mutation towards somatic parasitism provides the selective conditions for extensive allorecognition diversity. On the one hand, if allorecognition diversity did not build up fast enough, somatic parasites went to fixation; conversely, once parasites had gone to fixation no allorecognition diversity built up. On the other hand, the mere threat of parasitism could select for high allorecognition diversity, preventing invasion of somatic parasites. Moderate population viscosity combined with weak global dispersal was optimal for the joint evolution of allorecognition and protection against parasitism. Our results are consistent with the widespread occurrence of allorecognition in fungi and the low degree of somatic parasitism. We discuss the implications of our results for allorecognition in other organism groups.
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http://dx.doi.org/10.1016/j.fgb.2014.09.010DOI Listing
December 2014
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