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Fungal Genomes Tell a Story of Ecological Adaptations

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Fungal Genomes Tell a Story of Ecological Adaptations Folia Biologica et Oecologica 10: 9–17 (2014) Acta Universitatis Lodziensis Fungal genomes tell a story of ecological adaptations ANNA MUSZEWSKA Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Pawinskiego 5A, 02-106 Warsaw, Poland E-mail: [email protected] ABSTRACT One genome enables a fungus to have various lifestyles and strategies depending on environmental conditions and in the presence of specific counterparts. The nature of their interactions with other living and abiotic elements is a consequence of their osmotrophism. The ability to degrade complex compounds and especially plant biomass makes them a key component of the global carbon circulation cycle. Since the first fungal genomic sequence was published in 1996 mycology has benefited from the technolgical progress. The available data create an unprecedented opportunity to perform massive comparative studies with complex study design variants targeted at all cellular processes. KEY WORDS: fungal genomics, osmotroph, pathogenic fungi, mycorrhiza, symbiotic fungi, HGT Fungal ecology is a consequence of osmotrophy Fungi play a pivotal role both in encountered as leaf endosymbionts industry and human health (Fisher et al. (Spatafora et al. 2007). Since fungi are 2012). They are involved in biomass involved in complex relationships with degradation, plant and animal infections, other organisms, their ecological fermentation and chemical industry etc. repertoire is reflected in their genomes. They can be present in the form of The nature of their interactions with other resting spores, motile spores, amebae (in organisms and environment is defined by Cryptomycota, Blastocladiomycota, their osmotrophic lifestyle. Nutrient Chytrydiomycota), hyphae or fruiting acquisition and communication with bodies. The same fungal species symbionts and hosts are mediated by depending on environmental conditions secreted molecules. Fungi possess and in the presence of specific complex repertoires of secreted counterparts can display various molecules and membrane transporters lifestyles and strategies for example efficiently transporting specific entomopathogenic fungi are often compounds in both directions (Richards DOI: 10.2478/fobio-2014-0011 FOLIA BIOLOGICA ET OECOLOGICA & Talbot 2013). Their ability to degrade families. Expanded specific gene families plant debris, especially lignin and result from adaptation towards a specific cellulose makes them a key component lifestyle, carbohydrate degrading of the global carbon circulation cycle. enzymes are characteristic of plant Organism adaptation is achieved by gene related fungi whereas proteases of duplications leading to increased gene dermatophytes. Fungal genomics and 1KF genomes Fungi have been used as model Currently the 1000 Fungal Genomes organisms to study eukaryotic genetics Project (1KF) is aiming at sequencing for decades. Their compact genomes, two representatives of each fungal well studied biology and availability of family, everyone can nominate a molecular tools made them ideal sequencing candidate via a web service candidates for genome sequencing (a [http://genome.jgi.doe.gov/pages/fungi- PubMed search results in 30932 articles 1000-projects.jsf]. The available data related to “fungal genomes”, July 2014). create an unprecedented opportunity to The genomic sequence of Saccharomyces perform massive comparative studies cerevisiae published in 1996 was a with complex study design variants milestone in mycology and genetics targeted at all cellular processes. (Goffeau et al. 1996, Engel et al. 2014). Osmotrophic lifestyle and xenobiotic utilization Fungal genomes are much more genome of Ceriporiopsis subvermispora compact than plant and animal ones. shows its adaptation to lignin degradation Genes involved in a common metabolic in the expansions of laccases and pathway are often not only co-regulated manganese peroxidases (Fernandez- by the same transcription factor, but also Fueyo et al. 2012). co-localized in the genome. In some Gene organization, co-expression and cases this genomic proximity leads to co-regulation are essential when a gene cluster formation. Gene clusters are metabolic pathway includes steps with claimed as HGT (horizontal gene toxic intermediates. Such pathways are transfer) prone. Their direct acquisition sometimes conserved among distant leads to a straightforward evolutionary evolutionary groups. Interestingly benefit and outcompeting other microbes homologs of gene clusters with toxic (Richards & Talbot 2013). Since fungi intermediates which co-localize in fungi are osmotrophs their adaptation to new are often co-regulated in distant ecological niches means developing organisms, even in humans (McGary et strategies to degrade new substrates. al. 2013). It seems that clustering genes Mechanistically this is often achieved by involved in a common pathway with gene duplications with subsequent toxic intermediates is selected for substrate specificity alterations of the protection against the accumulation of resulting paralogs. As an example, the such intermediates. Genome size, genome richness, compactness According to a growing body of effective population size in the course of population genetics evidence increased evolution of eukaryotic populations. The genome sizes result from decreased drop in effective population size leads to 10 MUSZEWSKA A. FOLIA BIOLOGICA ET OECOLOGICA continuously growing complexity of Cryptomycota (James et al. 2013). genomes with expanded gene families, Genome sizes and gene numbers can be genes fragmented by introns and immediately elevated as a consequence surrounded by regulatory regions and of a whole genome duplication (WGD). mobile elements which eventually results The ohnologs (paralogs resulting from in greater overall genome sizes. All WGD) are known to evolve in an genome components seem to expand asymmetric manner, often leading to together. However, in fungi the coding gene loss or to neofunctionalizing. genome size is less variable than other WGDs have been detected in the genome components, with gene numbers evolutionary history of distant fungal between six and twenty thousand. Fungi lineages for example in Rhizopus vary in genome size and genome delemar (Mucorales) (Ma et al. 2009) compactness. Tuber melanosporum and Saccharomyces cerevisiae (Pezizomycotina) an ectomycorrhizal (Saccharomycetales) (Byrne & Wolfe forming fungus has a 125 Mb long 2007). genome with many transposable elements At least some fungi are said to (Martin et al. 2010) whereas plant possess a two-speed genome i.e. a pathogenic Taphrina deformans genome with housekeeping genes and the (Taphrinomycotina) has only a 14 Mb other genome with additional features, genome (Cissé et al. 2013). encoding specific effectors. The former, Micorosporidia have extremely compact primary genome is more compact, has a and reduced genomes which can be few and usually inactive mobile elements treated as a course book example of and introns. The latter, accessory genome adaptation to obligate intracellular is less gene dense, encodes many parasitism (Cuomo et al. 2012). The species/strain specific genes, has more peculiarities of obligate pathogen mobile elements, often from younger genomes cause problems in phylogeny families, sometimes still active and reconstruction. Microsporidia position intact. As an example rust fungi possess within fungi has been long discussed and one of the biggest genomes among fungi, currently they are considered as one of with areas abundant in mobile elements basal fungal lineages together with and short genes coding effector proteins. Effector proteins Short, secreted, cysteine rich proteins signalling (Plett et al. 2011). The are said to mediate interactions with a repertoire of effector proteins evolves host organism either a plant or an animal. much faster than of housekeeping genes Effectors play an immunomodulatory because it is in a constant ‘arms race’ role, both in pathogenic and symbiotic with the host immune system. These fungi, they can suppress host immune effectors are often clustered with response and thus facilitate tissue transposons which alter their expression. colonization (de Jonge et al. 2011, Host adaptation and host switching is Schmidt & Panstruga 2011). One of the often reflected in encoded effector plant defence mechanisms is via protein composition. Between closely jasmonic acid and mycorrhizal fungi like related taxa of Nectria haematococca and Laccaria bicolor (Agaricales) can Fusarium oxysporum this adaptation is promote mutualism by blocking the achieved by proteins encoded on GENOME ORGANIZATION AND FUNGAL LIFESTYLE 11 FOLIA BIOLOGICA ET OECOLOGICA supernumerary chromosomes carrying, specific chromosome regions are rich in among others, host specific effectors and repeat sequences, unique and duplicated mobile elements (Coleman et al. 2009, genes and reflect the species Ma et al. 2010). Conditionally habitat/niche. dispensable chromosomes and lineage Mobile elements in fungal genomes Lynch (Lynch & Conery 2003) groups and transposon types, LTR postulated that overall genome size retrotransposon (Muszewska et al. 2011), correlated with mobile element content YR retrotransposons (Muszewska et al. and decreasing effective population size. 2013), non-LTR retrotransposons In fungi, the genome size indeed (Novikova et al. 2009). These and other correlates well with the overall mobile analyses have showed that plant element content. Transposons (TE) are pathogens often possess large and repeat- DNA fragments capable of moving
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