Publications by authors named "Benjamin H Conlon"

10 Publications

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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

The Termite Fungal Cultivar Combines Diverse Enzymes and Oxidative Reactions for Plant Biomass Conversion.

mBio 2021 06 15;12(3):e0355120. Epub 2021 Jun 15.

Group of Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute (HKI), Jena, Germany.

Macrotermitine termites have domesticated fungi in the genus as their primary food source using predigested plant biomass. To access the full nutritional value of lignin-enriched plant biomass, the termite-fungus symbiosis requires the depolymerization of this complex phenolic polymer. While most previous work suggests that lignocellulose degradation is accomplished predominantly by the fungal cultivar, our current understanding of the underlying biomolecular mechanisms remains rudimentary. Here, we provide conclusive omics and activity-based evidence that employs not only a broad array of carbohydrate-active enzymes (CAZymes) but also a restricted set of oxidizing enzymes (manganese peroxidase, dye decolorization peroxidase, an unspecific peroxygenase, laccases, and aryl-alcohol oxidases) and Fenton chemistry for biomass degradation. We propose for the first time that induces hydroquinone-mediated Fenton chemistry (Fe + HO + H → Fe + OH + HO) using a herein newly described 2-methoxy-1,4-dihydroxybenzene (2-MHQ, compound 19)-based electron shuttle system to complement the enzymatic degradation pathways. This study provides a comprehensive depiction of how efficient biomass degradation by means of this ancient insect's agricultural symbiosis is accomplished. Fungus-growing termites have optimized the decomposition of recalcitrant plant biomass to access valuable nutrients by engaging in a tripartite symbiosis with complementary contributions from a fungal mutualist and a codiversified gut microbiome. This complex symbiotic interplay makes them one of the most successful and important decomposers for carbon cycling in Old World ecosystems. To date, most research has focused on the enzymatic contributions of microbial partners to carbohydrate decomposition. Here, we provide genomic, transcriptomic, and enzymatic evidence that also employs redox mechanisms, including diverse ligninolytic enzymes and a Fenton chemistry-based hydroquinone-catalyzed lignin degradation mechanism, to break down lignin-rich plant material. Insights into these efficient decomposition mechanisms reveal new sources of efficient ligninolytic agents applicable for energy generation from renewable sources.
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http://dx.doi.org/10.1128/mBio.03551-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8262964PMC
June 2021

GNPS-guided discovery of xylacremolide C and D, evaluation of their putative biosynthetic origin and bioactivity studies of xylacremolide A and B.

RSC Adv 2021 May 24;11(31):18748-18756. Epub 2021 May 24.

Chemical Biology of Microbe-Host Interactions, Leibniz Institute for Natural Product Research and Infection Biology, Hans Knöll Institute (HKI) Beutenbergstraße 11a 07745 Jena Germany

Targeted HRMS-GNPS-based metabolomic analysis of sp. X187, a fungal antagonist of the fungus-growing termite symbiosis, resulted in the identification of two lipopeptidic congeners of xylacremolides, named xylacremolide C and D, which are built from d-phenylalanine, l-proline and an acetyl-CoA starter unit elongated by four malonyl-CoA derived ketide units. The putative gene cluster was identified from a draft genome generated by Illumina and PacBio sequencing and RNAseq studies. Biological activities of xylacremolide A and B were evaluated and revealed weak histone deacetylase inhibitory (HDACi) and antifungal activities, as well as moderate protease inhibition activity across a panel of nine human, viral and bacterial proteases.
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http://dx.doi.org/10.1039/d1ra00997dDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8142242PMC
May 2021

Female-biased sex allocation and lack of inbreeding avoidance in termites.

Ecol Evol 2021 May 31;11(10):5598-5605. Epub 2021 Mar 31.

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

Sexually reproducing organisms face a strong selective pressure to find a mate and ensure reproduction. An important criterion during mate-selection is to avoid closely related individuals and subsequent potential fitness costs of resulting inbred offspring. Inbreeding avoidance can be active through kin recognition during mate choice, or passive through differential male and female-biased sex ratios, which effectively prevents sib-mating. In addition, sex allocation, or the resources allotted to male and female offspring, can impact mating and reproductive success. Here, we investigate mate choice, sex ratios, and sex allocation in dispersing reproductives (alates) from colonies of the termite . Termites have a short time to select a mate for life, which should intensify any fitness consequences of inbreeding. However, alates did not actively avoid inbreeding through mate choice via kin recognition based on genetic or environmental cues. Furthermore, the majority of colonies exhibited a female-biased sex ratio, and none exhibited a male-bias, indicating that differential bias does not reduce inbreeding. Sex allocation was generally female-biased, as females also were heavier, but the potential fitness effect of this costly strategy remains unclear. The bacterium , known in other insects to parasitically distort sex allocation toward females, was present within all alates. While is commonly associated with termites, parasitism has yet to be demonstrated, warranting further study of the nature of the symbiosis. Both the apparent lack of inbreeding avoidance and potential maladaptive sex allocation implies possible negative effects on mating and fitness.
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http://dx.doi.org/10.1002/ece3.7462DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8131773PMC
May 2021

Juvenile hormone pathway in honey bee larvae: A source of possible signal molecules for the reproductive behavior of .

Ecol Evol 2021 Jan 21;11(2):1057-1068. Epub 2020 Dec 21.

Faculty of Animal Science and Biotechnology University of Agriculture Sciences and Veterinary Medicine Cluj-Napoca Romania.

The parasitic mite devastates honey bee () colonies around the world. Entering a brood cell shortly before capping, the mother feeds on the honey bee larvae. The hormones 20-hydroxyecdysone (20E) and juvenile hormone (JH), acquired from the host, have been considered to play a key role in initiating reproductive cycle. This study focuses on differential expression of the genes involved in the biosynthesis of JH and ecdysone at six time points during the first 30 hr after cell capping in both drone and worker larvae of . This time frame, covering the conclusion of the honey bee brood cell invasion and the start of ovogenesis, is critical to the successful initiation of a reproductive cycle. Our findings support a later activation of the ecdysteroid cascade in honey bee drones compared to worker larvae, which could account for the increased egg production of in drone cells. The JH pathway was generally downregulated confirming its activity is antagonistic to the ecdysteroid pathway during the larva development. Nevertheless, the genes involved in JH synthesis revealed an increased expression in drones. The upregulation of gene involved in methyl farnesoate (MF) synthesis came into attention since the MF is not only a precursor of JH but it is also an insect pheromone in its own right as well as JH-like hormone in Acari. This could indicate a possible kairomone effect of MF for attracting the mites into the drone brood cells, along with its potential involvement in ovogenesis after the cell capping, stimulating initiation of egg laying.
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http://dx.doi.org/10.1002/ece3.7125DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7820148PMC
January 2021

A gene for resistance to the Varroa mite (Acari) in honey bee (Apis mellifera) pupae.

Mol Ecol 2019 06 5;28(12):2958-2966. Epub 2019 May 5.

Molecular Ecology, Institute of Biology/Zoology, Martin-Luther-University Halle-Wittenberg, Halle (Saale), Germany.

Social insect colonies possess a range of defences which protect them against highly virulent parasites and colony collapse. The host-parasite interaction between honey bees (Apis mellifera) and the mite Varroa destructor is unusual, as honey bee colonies are relatively poorly defended against this parasite. The interaction has existed since the mid-20th Century, when Varroa switched host to parasitize A. mellifera. The combination of a virulent parasite and relatively naïve host means that, without acaricides, honey bee colonies typically die within 3 years of Varroa infestation. A consequence of acaricide use has been a reduced selective pressure for the evolution of Varroa resistance in honey bee colonies. However, in the past 20 years, several natural-selection-based breeding programmes have resulted in the evolution of Varroa-resistant populations. In these populations, the inhibition of Varroa's reproduction is a common trait. Using a high-density genome-wide association analysis in a Varroa-resistant honey bee population, we identify an ecdysone-induced gene significantly linked to resistance. Ecdysone both initiates metamorphosis in insects and reproduction in Varroa. Previously, using a less dense genetic map and a quantitative trait loci analysis, we have identified Ecdysone-related genes at resistance loci in an independently evolved resistant population. Varroa cannot biosynthesize ecdysone but can acquire it from its diet. Using qPCR, we are able to link the expression of ecdysone-linked resistance genes to Varroa's meals and reproduction. If Varroa co-opts pupal compounds to initiate and time its own reproduction, mutations in the host's ecdysone pathway may represent a key selection tool for honey bee resistance and breeding.
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http://dx.doi.org/10.1111/mec.15080DOI Listing
June 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

The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honey bee (Apis mellifera) drones.

J Evol Biol 2018 06 17;31(6):801-809. Epub 2018 Apr 17.

Molecular Ecology, Institute of Biology/Zoology, Martin-Luther-University Halle-Wittenberg, Halle an der Saale, Germany.

The Red Queen hypothesis predicts that host-parasite coevolutionary dynamics can select for host resistance through increased genetic diversity, recombination and evolutionary rates. However, in haplodiploid organisms such as the honeybee (Apis mellifera), models suggest the selective pressure is weaker than in diploids. Haplodiploid sex determination, found in A. mellifera, can allow deleterious recessive alleles to persist in the population through the diploid sex with negative effects predominantly expressed in the haploid sex. To overcome these negative effects in haploid genomes, epistatic interactions have been hypothesized to play an important role. Here, we use the interaction between A. mellifera and the parasitic mite Varroa destructor to test epistasis in the expression of resistance, through the inhibition of parasite reproduction, in haploid drones. We find novel loci on three chromosomes which explain over 45% of the resistance phenotype. Two of these loci interact only additively, suggesting their expression is independent of each other, but both loci interact epistatically with the third locus. With drone offspring inheriting only one copy of the queen's chromosomes, the drones will only possess one of two queen alleles throughout the years-long lifetime of the honeybee colony. Varroa, in comparison, completes its highly inbred reproductive cycle in a matter of weeks, allowing it to rapidly evolve resistance. Faced with the rapidly evolving Varroa, a diversity of pathways and epistatic interactions for the inhibition of Varroa reproduction could therefore provide a selective advantage to the high levels of recombination seen in A. mellifera. This allows for the remixing of phenotypes despite a fixed queen genotype.
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http://dx.doi.org/10.1111/jeb.13271DOI Listing
June 2018

Draft genome of the fungus-growing termite pathogenic fungus (Ophiocordycipitaceae, Hypocreales, Ascomycota).

Data Brief 2017 Apr 8;11:537-542. Epub 2017 Mar 8.

Section for Organismal Biology, Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark.

This article documents the public availability of genome sequence data and assembled contigs representing the partial draft genome of . As one of the few known pathogens of fungus-farming termites, a draft genome of represents the opportunity to further the understanding of disease and resistance in these complex termite societies. With the ongoing attempts to resolve the taxonomy of the Hypocralaean family, more genetic data will also help to shed light on the phylogenetic relationship between sexual and asexual life stages. Next generation sequence data is available from the European Nucleotide Archive (ENA) under accession PRJEB13655; run numbers: ERR1368522, ERR1368523, and ERR1368524. Genome assembly available from ENA under accession numbers: FKNF01000001-FKNF01000302. Gene prediction available as protein fasta, nucleotide fasta and GFF file from Mendeley Data with accession doi:10.17632/r99fd6g3s4.2 (http://dx.doi.org/10.17632/r99fd6g3s4.2).
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http://dx.doi.org/10.1016/j.dib.2017.02.051DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5357700PMC
April 2017

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
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