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Twenty-Five Cultures of Lichenizing Fungi Available for Experimental Studies on Symbiotic Systems Tami R. Mcdonald, Ester Gaya

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Twenty-Five Cultures of Lichenizing Fungi Available for Experimental Studies on Symbiotic Systems Tami R. Mcdonald, Ester Gaya Twenty-five cultures of lichenizing fungi available for experimental studies on symbiotic systems Tami R. McDonald, Ester Gaya & François Lutzoni Symbiosis ISSN 0334-5114 Volume 59 Number 3 Symbiosis (2013) 59:165-171 DOI 10.1007/s13199-013-0228-0 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Symbiosis (2013) 59:165–171 DOI 10.1007/s13199-013-0228-0 SHORT COMMUNICATION Twenty-five cultures of lichenizing fungi available for experimental studies on symbiotic systems Tami R. McDonald & Ester Gaya & François Lutzoni Received: 12 November 2012 /Accepted: 22 January 2013 /Published online: 24 March 2013 # Springer Science+Business Media Dordrecht 2013 Abstract In this study we describe the techniques used to 1 Introduction culture 25 mycobionts spanning three classes and five orders of the leotiomyceta (Ascomycota). We find that five media, in- Attempts to culture the fungal and algal components of lichens cluding potato-carrot, malt extract-yeast extract (MY), Bold’s began almost concomitantly with the field of lichenology. As basal medium with nitrogen (NMBBM), oatmeal, and yeast early as the 1880s, Bonnier (1887, 1889)andStahl(1877) extract with supplements (YES), are sufficient to induce asco- separately reported success in culturing lichen fungi (Stocker- spore germination of many lichenizing fungi and are also Wörgötter 2001). Nearly a century later, Ahmadjian (1966, suitable for maintaining growth of the culture over the long 1973) did much to advance culturing techniques for lichenizing term. Regular physical disruption of the cultures in liquid media fungi, introducing and refining the spore-shot method is recommended to stimulate continued growth. Genomes of (Ahmadjian 1973). Additionally, cultures have been success- five of these lichen-forming fungal strains have been se- fully isolated from soredia (e.g. Armaleo and May 2009)and quenced. The identity of each culture was confirmed by se- thallus fragments (Yamamoto et al. 1985; Armaleo 1991; quencing the nuclear ribosomal internal transcribed spacer Yamamoto et al. 1993). However, despite the many reports of (ITS) or the mitochondrial small subunit (mitSSU) from each cultures of isolated fungal partners of lichens (e.g., Oliver et al. strain. Additionally, the level of sequencing in terms of total 1989;Jahns1993; Yamamoto et al. 1993; Crittenden et al. number of genes sequenced for each taxon is provided. All 1995; Stocker-Wörgötter 2001, 2002; Sangvichien et al. fungal cultures have been deposited in public culture collec- 2011), few cultures of lichenizing fungi are publicly available tions and, therefore, are available to the scientific community in culture banks compared to the prevalence of yeasts and non- for conducting in vitro experiments. lichenizing filamentous fungi in culture collections (see CBS- KNAW database as an example), with the exception of 38 Keywords Culture . Lichens . Fungi mycobiont cultures from Ahmadjian in the American Type Culture Collection. One major reason for the comparative dearth of publicly Tami R. McDonald and Ester Gaya were equally contributing authors. available cultures of lichenizing fungi is that these fungi are tedious to isolate. Although culture conditions and nutritional Electronic supplementary material The online version of this article (doi:10.1007/s13199-013-0228-0) contains supplementary material, requirements have been reported for many lichenizing fungi which is available to authorized users. (e.g., Bubrick 1988; Stocker-Wörgötter 1991; Crittenden et al. 1995; Sangvichien et al. 2011), the culture conditions for most T. R. McDonald (*) Department of Microbiology, University of Minnesota, lichenizing fungi, especially those with slow growth rates, MMC 196 420 Delaware St. SE, remain unknown. In addition, if culturing conditions are Minneapolis, MN 55455, USA known, it is not trivial to establish a pure culture since even e-mail: [email protected] when external fungal and bacterial contaminants are scrupu- E. Gaya : F. Lutzoni lously excluded, within the thallus of a lichen are several Biology Department, Duke University, Durham, NC, USA endolichenic fungi (Arnold et al. 2009;U’Ren et al. 2010), Author's personal copy 166 T.R. McDonald et al. which may grow faster than, or as slowly as, lichenizing fungi. potentially shedding light on how many independent origins These contaminants can grow out of thallus fragments if these of lichenization there have been in the evolution of filamen- are used to initiate the culture, and thus it is possible that some tous ascomycetes. A novel aspect of this project is that the reports of the successful culture of lichenizing fungi were fungal and algal cultures for each lichen are derived from the actually describing endolichenic fungi. The great majority of same thallus, so that the genomes represent the symbiosis as it these endolichenic fungi are filamentous ascomycetes in the exists in nature. Pezizomycotina, the same subphylum that includes all lichen- The fungal and algal genomes of the lichen Cladonia forming Ascomycota species (Arnold et al. 2009). Further, the grayi have revealed several interesting aspects of lichen- lichen symbiosis is obligate in nature for most lichenizing ization. The possibility of horizontal gene transfer between fungi as well as for several of the most common lichenizing the fungus and alga was explored by examining the algal algae, suggesting that it might not be possible to bring certain genome for genes of fungal origin and the fungal genome lichenizing fungi into pure culture. for genes of putative algal origin. No obvious horizontal Another major reason why so few cultures are available is gene transfer from the fungus to the alga was evident in the that once a pure culture is obtained, it may be difficult to algal genome, but two plant-like genes were discovered in maintain. The slow growth rates of lichenizing fungi in culture the fungal genome. Both of these genes encoded ammonium mean that the lichenizing fungus is readily outgrown by even transporters (McDonald et al. 2012). Several additional slow-growing contaminants. In addition, lichenizing fungi lichenizing fungi were surveyed for the presence of these grow in liquid culture for only a few weeks before appearing ammonium transporters to pinpoint the evolutionary timing to lapse into a static state. Once cultures have reached this of this horizontal gene transfer event. Cultures of the lichen stage, they must be physically disrupted (for example, in a mycobionts were necessary to ensure that the plant-like blender) in order to stimulate growth (Ahmadjian 1973). ammonium transporters amplified were indeed from the Furthermore, each transfer and every further manipulation fungal genomes and could not be attributed to the lichen presents a possibility of contamination. alga. We have isolated the mycobionts of 25 lichens in axenic In the DNA methylation project, the report of widespread culture. These cultures were obtained in the context of three DNA methylation of the fungal genome exclusively in the projects: (1) the Assembling the Fungal Tree of Life (AFToL symbiotic state of Cladonia grayi (Armaleo and Miao 1999) 2) project; (2) a project at Duke University and Pacific was explored by bisulfite sequencing of the free-living and Northwest National Laboratory to sequence the genomes of symbiotic genomes of both the fungus and the alga com- the fungal and algal partners of three lichens; and (3) a Ph.D. prising the lichen Cladonia grayi. dissertation focusing on the molecular evolution of ammoni- Here, we describe the methods used to culture lichen um transporters and DNA methylation in lichen-forming fungi mycobionts from 25 lichens in three classes of fungi and five (McDonald 2011). orders, including the Acarosporales, Lecanorales, Ostropales The Assembling the Fungal Tree of Life (AFToL 2) (Lecanoromycetes), Pyrenulales (Eurotiomycetes), and project involved the sequencing of 21 new protein-coding Trypetheliales (Dothideomycetes) to produce large-scale cul- genes from 63 species representing all main lineages of tures suitable for providing the requisite amount of DNA for lichen-forming fungi and allied non-lichenized fungi. In genome sequencing. The main goal of this note is to report the most cases, amplification of DNA from cultures of lichen- strains from these three studies that have been successfully izing fungi rather than from thalli was deemed the best isolated and deposited in publicly available culture banks for option, as it ruled out the possible amplification of DNA future research on lichen symbiotic systems. We also report from contaminating endolichenic fungi. Additionally, cul- the number of genes sequenced or average genome coverage turing was also necessary to generate sufficient material to for each culture. allow amplification
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