Archive for August, 2010

Living Stones

August 29th, 2010

Villaron - pierre colorée de lichens

Together with the mycorrhizal symbiosis, the lichen symbiosis has fascinated biologists for decades.

Lichens are composite organisms consisting of a fungus (the mycobiont) interacting with a photosynthetic partner (the photobiont), an algae or a cyanobacterium, to form a mutualistic interaction. These chimeric organisms are found in most ecosystems, including in some of the most extreme environments — deserts, rocky coasts, mountains, artic tundra, … . They are also abundant as epiphytes on trees, on bare rocks, such as walls, benches and tombstones. The morphology and physiology of lichens are very different from those of the free-living fungi and algae, but very little is known on the signals, genes and proteins involved in the complex symbiotic interactions.

The genomes of two ectomycorrhizal symbionts, the basidiomycete Laccaria bicolor and the ascomycete Tuber melanosporum, are now available to study the evolution of fungal symbiosis. No lichen genome was available to date to investigate how this other major fungal symbiosis evolved. This is thus great to see that the 36-Mb genome of the lichen Cladonia grayi has been sequenced (by 454 and Illumina). C. grayi is a member of the Cladoniaceae, a well-studied world-wide family of stalked-cup lichens classified within the Lecanoromycetes, a class that includes more than 70% of the lichen-forming fungal diversity. The 60 Mb genome of the Asterochloris photobiont associated with C. grayi has also been sequenced. Asterochloris sp. a single celled member of the largest family of lichen-forming green algae, the Trebouxiaceae.

We are excited to be part of the Cladonia Genome Consortium leaded by Daniele Armaleo and François Lutzoni (Duke University).

Photo: A lichen community on a stone wall in the Villaron hamlet (Haute-Maurienne, France). © F Martin

Histoire de Fourmis … suite: Ant Genomes

August 29th, 2010


Symbioses between plants and fungi, fungi and ants, and ants and plants all play important roles in ecosystems. For those interested by ant ecology and biology, and their interaction with plants, I would recommend reading the paper from Defossez et al. on Ant‐plants and fungi: a new threeway symbiosis‘ published on March 11, 2009 in the New Phytologist. For further ant reading go to the comparative genomics paper published by Bonasio et al. in the 27 August 2010 issue of Science. A collaborative research consortium involving scientists from the US and China report that they have sequenced the genomes of two ant species: Harpegnathos saltator, known as Jerdon’s jumping ant, and the Florida carpenter ant, Camponotus floridanus.

By comparing the genome structure and gene repertoire of the two ant species, and analyzing their transcriptome profiling in different castes, the team obtained clues about gene regulation and epigenetic processes underlying diverse physical and behavioral features in these ant species. They identified up-regulation of telomerase and sirtuin deacetylases in longer-lived H. saltator reproductives, caste-specific expression of microRNAs and SMYD histone methyltransferases, and differential regulation of genes implicated in neuronal function and chemical communication. Their findings provide clues on the molecular differences between castes in ants paving the way for further investigations on everything from brain function and behavior to aging.

Photo: Florida Carpenter Ant (by Alex Wild)

Aging in Long-Lived Aspen

August 28th, 2010

Trembles - Plateau de Larina

In my series Tree Lover stories:

Ally D, Ritland K, Otto SP (2010) Aging in a Long-Lived Clonal Tree. PLoS Biol 8(8): e1000454. doi:10.1371/journal.pbio.1000454

Author Summary: Aging has been demonstrated in many animals and even in bacteria, but there is little empirical work showing that clonal plants age. Evidence for aging in long-lived perennials is scarce because it typically requires survivorship or fecundity schedules from long-term demographic data. Given the extreme lifespan of many long-lived perennials, it is difficult to follow cohorts of individual clones to collect late-life survivorship or fertility. Our work offers a novel approach for obtaining late-life demographic data on a clonal species by using genetic data to estimate the age of individual clones. We studied plant clones in a natural population of trembling aspen, which grows clonally via lateral root suckers. By coupling estimates of each clone’s age with a measure of its male reproductive performance, we show that long-lived plant clones do senesce. Although clonal plants have the capacity for continued growth and reproduction even late in life, mutations that reduce fertility can accumulate because selection on sexual fitness is absent during clonal growth, potentially explaining senescence in this species.

Photo: © F Martin

Graveyards on the Move

August 28th, 2010

Cemetery_4Zombie Ants‘, ‘Graveyards on the Move‘ … fungi can make the headlines of newspapers, such as The Guardian, and blog posts (Ancient Zombie Ants, Fungal Parasites & Zombie Ants, Genetics and Behavior, Cordyceps and Nature’s parasitic relationship with it). They referred to the parasitoid Cordyceps fungi (Ascomycota, Pezizomycotina, Sordariomycete, Hypocreales) — a genus that includes about >600 described species. All Cordyceps species are endoparasitoids, mainly on insects and other arthropods.

Jason’s recent tweet  ‘A fun blog post & paper review on Cordyceps entitled “fungal parasites & zombie ants“‘ reminded me one of the more stunning sections of the 2006 BBC’s documentary series Planet Earth showing an ant being preyed on by Cordyceps — you can check out this segment narrated by Sir David Attenborough on YouTube — . Fruiting body of the infecting cordyceps erupting from the ant head and the mushrooming bodies of dead insects are frightening, but so beautiful.

The fungus Ophiocordyceps unilateralis, which is pan-tropical in distribution, causes infected worker ants to leave their nest and die under leaves in the understory of tropical rainforests. Cordyceps spores glue to foraging Carpenter ants (Camponotus leonardi), germinate on the insect cuticule and the fungal hyphae then grows inside the ant body where it releases chemicals that affect host behaviour. Some ants leave the colony and wander off to find fresh leaves on their own, while others fall from their tree-top havens on to leaves nearer the ground. The final stage of the parasitic infection (which may last 3 to 6 days) is the most macabre. In their last hours, infected ants — the zombies — move towards the underside of the leaf they are on and clamp their mandibles in a “death grip” around the central vein, immobilising themselves and locking the fungus in position. Very high densities of dead ants can occur underside of leaves leading to patches. Spores are too large to be wind dispersed and instead fall directly to the ground where they produce secondary spores that infect foraging Carpenter ants as they walk over them.

In a study published last year in PLoS OneMaj-Britt Pontoppidan and her colleagues have shown that the Cordyceps parasitoid not only affects individual ants, but they can also structure the entire host population of a tropical forest in Thailand in terms of its distribution in time and space, and then influence their own distribution: the ‘parasite’s ‘extended phenotype‘. It appeared that the dead ant bodies weren’t randomly distributed in the Thai rainforest floor. Instead they were in large aggregations (the so-called ‘graveyards‘) of up to 26/m2, separated by corpse-free zones. The dead ants had locked onto the undersides of leaves – an example of how the fungus influences its host’s behaviour. The distribution of dead ants appeared to be related to temperature and absolute humidity – things which could influence the survival of fungal spores and thus the chances of an individual ant picking up the infection.

Ant death-grip leaf scars have been documented on 48 Ma fossil leaves, indicating the antiquity of this behaviour (Hughes et al. (2010) Biology Letters online).

Fungal parasites and symbionts play an important role in structuring host plant populations. This study  showed that they also affect animal populations … what about human behavior? (see: the Human Afflicting Strain of Cordyceps Fungus).

BTW, Thanks to its medicinal properties, mushroom hunters in Tibet can earn $900 dollars for an ounce of cordyceps.

Pontoppidan M-B, Himaman W, Hywel-Jones NL, Boomsma JJ, Hughes DP (2009) Graveyards on the Move: The Spatio-Temporal Distribution of Dead Ophiocordyceps-Infected Ants. PLoS ONE 4: e4835. doi:10.1371/journal.pone.0004835

Hughes, DP,  Wappler , T & Lanadeira, CC (2010) Ancient death-grip leaf scars reveal ant-fungal parasitism. Biology Letters. Published online before print August 18, 2010, doi:10.1098/rsbl.2010.0521


Photo: Cambridge Graveyards, UK © F Martin & A carpenter ant (Camponotus leonardi) whose body has been consumed by the fungus Ophiocordyceps © David P Hughes

Chitin Sequestration

August 25th, 2010

ch25f45One of the major driving forces of evolution on our green planet is the constant arms race between plants and the microbial pathogens that crawl on their leaves and roots, and then infect them. During humid conditions, conidia of the biotrophic fungus Cladosporium fulvum (leaf mold) germinate on the lower leaf surface of tomato plants and produce runner hyphae that enter the host through open stomata. In a compatible interaction hyphae remain strictly intercellular without penetrating the mesophyll cells and no haustoria or other specialised feeding structures are produced. Typical symptoms of the disease are yellow and chlorotic spots that gradually become necrotic and are visible on the upper side of the infected leaves (see photo). The C. fulvum-tomato interaction strictly obeys the gene-for-gene concept, implying that for every pathogen avirulence gene ( Avr ) there is a matching cognate plant resistance gene (R) that mediates recognition of the pathogen by the host. This interaction has extensively been investigated by Pierre de Wit’s group at Wageningen University.

One of the ways tomato plants sense infections by C. fulvum hyphae is by detecting the fungal cell wall chitin oligosaccharides released by induced plant chitinases residing in the host apoplast. In response, the fungus has evolved ‘stealthing’ strategies to evade detection. In the last issue of Science,  De Jonge et al. have now characterized one such mechanism in C. fulvum, mediated by the effector protein Ecp6. Secreted Ecp6 is capable to bind to chitin oligosaccharides that are released upon degradation of the fungal cell wall and sequester them so that they are not detected by tomato chitin receptors. Proteins with domain structure similar to Ecp6 are conserved throughout the fungal kingdom, which suggests that chitin sequestration may represent a general mechanism used by fungi to evade immune detection. Interestingly, one of the most highly upregulated symbiosis-induced gene of the ectomycorrhizal Tuber melanosporum is also coding for a secreted LysM protein (Martin et al., 2010), suggesting that mycorrhizal symbiont may use a similar mechanism during infection to conceal the hyphae from the host.

R. de Jonge, H. P. van Esse, A. Kombrink, T. Shinya, Y. Desaki, R. Bours, S. van der Krol, N. Shibuya, M. H. A. J. Joosten, B. P. H. J. Thomma (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329, 953–955.

Photo: Tomato leaves infected by the leaf mold fungus Cladosporium fulvum. © Molecular Biology of the Cell, 4th edition,Bruce Alberts, Alexander Johnson, Julian Lewis, Martin Raff, Keith Roberts, and Peter Walter, New York: Garland Science; 2002.

Friend or foe? … a Sweet Story

August 16th, 2010

Sans titreThe sky is overcast with clouds and the rain is ceaseless‘ in Gitanjali by Rabindranath Tagore.

Mid-Summer: Across Lorraine, this is generally the hottest month of the year, and when most everyone is headed to a beach or the mountains to look for a little respite. No scorching mid-Summer heat this year. Over the week-end, the sky was pouring with rain and the sun never shone from dawn to dusk. It poured with rain the entire night.

Well, I take this opportunity to get back to outstanding papers. The study of GH32 invertases in fungi from Jerri Parent, together with Tim James and Andy Taylor, was worth re-reading. In this BMC Evolutionary Biology paper, they tested for occurrence of the glycosyl hydrolase family 32 (GH32) genes in all available fungal genomes and an additional 149 species representing a broad phylogenetic and ecological range of biotrophic fungi. This GH32 family, containing mostly invertases, is crucial for plant-interacting fungi. Sucrose is the primary metabolite used by most plants to translocate carbon throughout their tissues, and its abundance within plants makes it a valuable carbon source for the many fungi that are obligate plant associates. To acquire the host sucrose, colonizing fungi must possess the necessary enzymes, such as extracellular invertase(s), to split sucrose into its constituent monosaccharides, glucose and fructose.

Ancestral state reconstruction of GH32 gene abundance showed a strong correlation with nutritional mode (saprobic, endophytic, mutualist, pathogenic). Expansion of gene families was observed in several clades of pathogenic filamentous Ascomycota species. GH32 gene number was negatively correlated with animal pathogenicity and positively correlated with plant biotrophy (e.g. Puccinia graminis), with the notable exception of mycorrhizal taxa (e.g. Laccaria bicolor). Few mycorrhizal species were found to have GH32 genes as compared to other guilds of plant-associated fungi, such as pathogens, endophytes and lichen-forming fungi. GH32 genes were also more prevalent in the Ascomycota than in the Basidiomycota.

We noticed in our Nature paper the lack of invertase in the ectomycorrhizal L. bicolor suggesting that this symbiont depends on its host plant to provide glucose in exchange for nitrogen. I have checked the presence of the extracellular invertase in our draft genome sequences of L. amethystina and Glomus intraradices, and the 454 transcripts of Lactarius quietus and Pisolithus microcarpus. None of these ECM fungi have a gene coding for this enzyme, whereas the poplar rust, Melampsora larici-populina has two sequences similar to the wheat rust Puccinia graminis GH32s. Intriguingly, the genome of the ectomycorrhizal ascomycete, Tuber melanosporum — the Black Truffe of Perigord — contains a gene encoding a GH32 enzyme, suggesting that the truffle may act as a scavenger instead of being a true mutualist. However, the corresponding transcript is lowly expressed in free-living mycelium, fruiting body and ectomycorrhiza according to our NimbleGen oligoarray and RNA-Seq transcript profilings.

As stressed by Parent et al. “Reliance on plant GH32 enzyme activity for C acquisition in these [ECM] symbionts supports earlier predictions of a general absence of invertase in mycorrhizal fungi, and a highly evolved mutualistic relationship between plants and mycorrhizal fungi, a remarkable scenario in light of the high degree of phylogenetic diversity spanned by mycorrhizal fungal taxa. Whether the plant host is able to detect fungal invertase activity and use such a signal to differentiate antagonistic from mutualistic biotrophic symbionts is a completely speculative, though plausible hypothesis.”

Parrent et al. (2009) Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses. BMC Evolutionary Biology 9:148 doi:10.1186/1471-2148-9-148.

Photo: Lorraine Big Sky © F Martin

Genome Erosion in the Pond

August 16th, 2010

azollaThe conversion of a free-living micro-organism into a domesticated organelle has been a crucial event during the evolution of Life on our planet, and mitochondria and chloroplasts have become virtually indispensable components of eukaryotic life. It is now textbook knowledge that an ancient cyanobacterial incorporation into a eukaryotic organism led to the evolution of plastids (chloroplasts) and subsequently to the origin of the plant kingdom. Still very little is know on how the engulfed genomes have evolved within their hosts. The process of genome shrinkage appears to be the rule in the in the obligate bacterial endosymbiont Buchnera aphidicola colonizing insects, such as aphids (van Ham et al., 2003).  In a recent issue of PLoS ONE, Ran et al. have sequenced the genome of Nostoc azollae, a nitrogen-fixing symbiont of the water fern Azolla filiculoides and they suggest that this cyanobacterium may have been partly domesticated by its host. In this symbiotic system, N. azollae is residing extracellularly in an endosymbiosis with its host plant, the water-fern A. filiculoides. the cyanobacterium lacks autonomous growth and is vertically transmitted between plant generations.

Birgitta Bergman’s group noted that there appears to have been co-evolution between the green host and its bacterial symbiont, as revealed in the intricate means by which Azolla maintains cyanobacterial colonies through successive generations. Furthermore, hallmarks of genome reduction in the symbiont, such as excessive pseudogenization, were identified, and the pattern of gene losses resembled that of another plant symbiont, rather than closely related, free-living cyanobacteria. Several basic metabolic processes such as glycolysis, replication, and nutrient import had suffered losses, yet nitrogen-fixing pathways had remained intact. This apparent streamlining of the genome indicates that progress toward a full mutualism between the plant and the cyanobacterium may be well under way.

The process of genome reduction, described extensively for intracellular bacterial symbionts and parasites of insects, is thus able to also influence the genomes of extracellular symbiotic bacteria.

Ran et al. (2010) Genome Erosion in a Nitrogen-Fixing Vertically Transmitted Endosymbiotic Multicellular Cyanobacterium. PLoS ONE 5, e11486.

Van Ham et al. (2003) Reductive genome evolution in Buchnera aphidicola. PNAS 100: 581-586.

Photo: Azolla pinnata and Azolla filiculoides. Thanks to eyeweed.

Tree Tale

August 15th, 2010

kiri tree“Have you heard the Taoist tale of the Taming of the Harp?

Once in the hoary ages in the Ravine of Lungmen stood a Kiri tree*, a veritable king of the forest. It reared its head to talk to the stars; its roots struck deep into the earth, mingling their bronzed coils with those of the silver dragon that slept beneath. And it came to pass that a mighty wizard made of this tree a wondrous harp, whose stubborn spirit should be tamed but by the greatest of musicians. …”

Okakura Kakuzo: The Book of Tea — Chapter Five: Art Appreciation

cited by Arianna Savall in her last CD ‘Peiwoh‘ inspired on the taoist legend of this old Eastern harp.

* Paulownia

Painting by Chad Beatty. If you like stunning tree paintings, visit his site ‘Art of Chad Beatty’.

Soil Metagenomics 2010

August 15th, 2010

401px-Braunschweig-burgplatz_1Christoph Tebbe is organizing the next International Symposium on Soil Metagenomics at the Johann Heinrich von Thünen-Institute (vTI) Forum in Braunschweig (Germany) on December 08–10, 2010. An objective of this symposium is to discuss the future applications of next generation sequencing to address the complex soil ecosystems.

Photo: © Burgplatz in Braunschweig, Germany by Matthias Prinke.


August 9th, 2010

noise1The 454 sequencing technology is revolutionising the field of microbial ecology by providing a means to sequence millions of partial PCR-amplified rDNA sequences (16S, ITS) rapidly and efficiently. However, this new approach brought new problems to a field fraught with potential sources of bias.

Nick Loman (Pathogens: Genes & Genomes) attended a workshop on 16S analysis by using the PyroNoise software written by Chris Quince at the University of Glasgow. He summarized a few notes on this workshop hoping they will be useful to the wider community. If you are a 454 user, you SHOULD read this blog post, ‘Come on feel the pyronoise‘.

A Virus in a Fungus in a Plant

August 8th, 2010

YNPFor those interested by plant endophytes (see previous post on poplar endophytes), get back to Márquez’s paper published in Science in 2007. The authors showed that mutualistic association between the fungal endophyte Curvularia protuberata and its host plant, the tropical panic grass from geothermal soils Dichanthelium lanuginosum allows both organisms to grow at high soil temperatures (65°C) in Yellowstone National Park. This stress tolerance requires the presence of a dsRNA  virus colonizing the fungal endophyte. Fungal isolates cured of the virus are unable to confer heat tolerance, but heat tolerance is restored after the virus is reintroduced. The virus-infected fungus confers heat tolerance not only to its native monocot host but also to a eudicot host, which suggests that the underlying mechanism involves pathways conserved between these two groups of plants.

Recently, complex tripartite symbioses have also been found among arthropods, bacteria, and mutualistic bacteriophages.

Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A Virus in a Fungus in a Plant: Three-Way Symbiosis Required for Thermal Tolerance. Science 315, 513 – 515.

Photo: ©