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Success in the Isolation and Axenic Culture of Anaptychia Ciliaris (Physciaceae, Lecanoromycetes) Mycobiont

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Success in the Isolation and Axenic Culture of Anaptychia Ciliaris (Physciaceae, Lecanoromycetes) Mycobiont mycoscience 56 (2015) 351e358 Available online at www.sciencedirect.com journal homepage: www.elsevier.com/locate/myc Full paper Success in the isolation and axenic culture of Anaptychia ciliaris (Physciaceae, Lecanoromycetes) mycobiont M. Carmen Molina a,*, Pradeep K. Divakar b, Natalia Gonzalez a a Departamento de Biologı´a y Geologı´a (Area de Biodiversidad y Conservacion), ESCET, Universidad Rey Juan Carlos, Mostoles, 28933 Madrid, Spain b Departamento de Biologı´a Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, 28040 Madrid, Spain article info abstract Article history: The aim of this study was to evaluate the optimum conditions for culturing Anaptychia Received 30 July 2014 ciliaris mycobionts in vitro and analyzing their ontogenetic development while in culture. Received in revised form After the testing of two germination and four development media, results of germination 29 October 2014 and growth were evaluated. We here recommend the use of basal medium without addi- Accepted 29 October 2014 tional carbon source for germination process. Mycobiont growth was possible in all organic Available online 23 February 2015 media tested. The maximum mycobiont growth was observed in Lilly and Barnet medium enriched with 3% glucose. Keywords: © 2014 The Mycological Society of Japan. Published by Elsevier B.V. All rights reserved. Aposymbiotic cultures Development Lichen Morphogenetic differences Ontogeny dyes for cotton and wood since the Middle Ages. Additionally, 1. Introduction lichens have frequently been used in the fragrance industry, in medical and pharmacology applications, as biomonitors A lichen is defined as an obligate symbiosis of a fungus (usu- and bioindicators of air quality, and as bioattenuation agents ally Ascomycota) and a unicellular or filamentous green alga (e.g., Luo et al. 2010; Aberoumand 2011; Favelo-Longo and (around 85% of all lichen species), a cyanobacterium (around Piervittori 2012; Wang et al. 2012; Kosanic et al. 2013). These 10%), or both (about 5%; Showman and Flenniken 2004). Li- are just a variety of examples of past, current, and potential chens are often poorly investigated in fields such as biotech- applications of these complex organisms. nology; however, lichens have traditionally been used by It is difficult to find out precisely how and where lichen humans (Muggia et al. 2009; Molnar and Farkas 2010). Chem- materials are collected and what species are collected for ical substances from lichens have been a source of important commercial purposes due to lack of documentation and public * Corresponding author. Tel.: þ34 914887090; fax: þ34 916647490. E-mail address: [email protected] (M.C. Molina). http://dx.doi.org/10.1016/j.myc.2014.10.003 1340-3540/© 2014 The Mycological Society of Japan. Published by Elsevier B.V. All rights reserved. 352 mycoscience 56 (2015) 351e358 information, given that the collection of these materials is cultured in vitro (Crittenden et al. 1995), but little is known often illegal. It is estimated that several thousand tons of li- about its development in aposymbiotic culture or how to in- chens are processed every year worldwide (Joulain and crease biomass yield for more extensive studies. Tabacchi 2009a, b). Such extensive exploitation, as well as The primary aim of this study was to analyze the ontoge- deterioration or destruction of habitat and environmental air netic development of the A. ciliaris mycobiont from sporula- pollution are the main causes of major loss of lichen diversity tion to formation of aposymbiotic aggregates (mycobiont (Upreti et al. 2005) and could be a threat to lichen species like colonies) and to find optimal protocols to find favorable con- Anaptychia ciliaris. ditions for mycobiont development in vitro cultures. The In order to increase the production of lichen substances for attainment of this goal will allow us to obtain total DNA suf- commercial applications, provide a sustainable harvestable ficient for complete genome sequencing of this fungal source, and reduce as much as possible the impact on natural mycobiont. communities, several new research areas and production methods have been investigated: whole and aposymbiotic culture (Yamamoto et al. 1987a; Yoshimura et al. 1989; 2. Materials and methods Stocker-Worg€ otter€ 2007), in vitro biosynthesis (Stocker- Worg€ oter€ and Elix 2006), bioreactor systems (Blanco et al. 2.1. Lichen materials 2002), and the cloning and expression of PKS (polyketide synthase) gene, a key enzyme in the synthesis of phenols Three well-developed Anaptychia ciliaris thalli growing on (Gagunashvili et al. 2009). However, in most cases these Fagus sylvatica were collected at Hayedo de Montejo, Madrid, biotechnology techniques have not gone beyond the experi- Spain (N 41 040 6300 W03 290 6500, alt. 1290 m) on Oct 15th, 2010. mental stages, since problems such as no spore discharge or Apothecia density on thalli was calculated as number of germination, difficulties in the selection of suitable culture apothecia by cm2, using total surface of all thalli. medium, and very slow growth of mycobionts under apo- symbiotic conditions have been frequent (Crittenden et al. 2.2. Isolation and culture 1995; McDonald et al. 2013). Contaminations have also been particularly problematic if they are from endolichenic fungi. Twenty apothecia from one thallus (MAF-Lich 17758) were Different composition of mycobiont substances in culture and selected to be analyses. The apothecia were used immediately in nature (Molina et al. 2003) and stagnation in the early stages after their collection, because freshness is an important factor of development in experimental resynthesized lichen and in dispersal and germination success of spores (Sangvichien limited ability to keep whole-lichen thalli and aposymbiotic et al. 2011). The apothecia had intermediate diameters culture alive for an extended time are drawbacks frequently (about 5 mm in diameter) to ensure, as far as possible, sexual described (McDonald et al. 2013). In spite of these common maturity (Molina et al. 1997). All apothecia were washed and complications, an important number of in vitro cultures (be- carefully cleaned following the protocols published in Molina tween 30 and 40% of species that have been tried) from crus- and Crespo (2000). The fungi were grown from discharged tose and foliose lichens have been successfully obtained but spores following the inversed Petri dish methods of only to the early stages of development (Crittenden et al. 1995; Ahmadjian (1993). Ten clean ascomata were attached to the Jeon et al. 2009; Sangvichien et al. 2011). Therefore, it is inner side of Petri dish lids with petroleum jelly. The bottom necessary to improve techniques and protocols for artificial part of the Petri dishes contained inorganic Basal Bold me- production of lichens for scientific as well as economic pur- dium [BBM; Deason and Bold (1960)]. The other ten ascomata, poses, and also to expand the number of species available as were arranged similarly for organic media, 1% glucose BBM aposymbiotic cultures in order to obtain standardized large- (w/v) [1% G-BBM; Behera and Makhija (2001)]. The Petri dishes scale production of compounds unique to lichens. were inverted over the lids and the ascospores were allowed In this experimental study we used A. ciliaris as a model to discharge upwards onto the medium for 24 h at 18e20 Cin due to its broad applications. This is a fruticose lichen that the dark (Molina and Crespo 2000). After this time, the reproduce sexually by ascospores and it is commonly growing apothecia were removed to avoid contaminations and new as an epiphyte in Europe. It belongs to the family Physciaceae lids were placed. in Ascomycota (Divakar et al. 2007). This species has been To estimate the percentage of apothecia capable of ejecting used in biomonitoring of atmospheric pollution (Borg and ascospores, we used all the apothecia. However, to assess Aronsson 2004), in traditional alcoholic production of brandy germination in BBM and 1% G-BBM, we could only use three (see Smith 1921), and as a potential natural source of antiox- apothecia for each medium, after eliminating those apothecia idant and antibiotic (Rankovic et al. 2010). It is also a model for contaminated by bacteria or fungi. Seven days after germi- the study of symbiotic systems in algae, and therefore it is of nation, 36 randomly selected and isolated uncontaminated particular interest to get enough biomass of this mycobiont multispores from BBM media were transported to and sub- available for future experimental studies on symbiotic sys- cultured on four organic different media: 2% glucose BBM (w/ tems. Trebouxia decolorans (the A. ciliaris algal photobiont) v) [2% G-BBM; Behera and Makhija (2001)]; Lilly and Barnet genome has recently been sequenced to analyze horizontal medium enriched with 3% glucose (w/v) [3% G-LBM; according gene transfer from fungi to lichen algae (Beck et al., pers. to Lilly and Barnett (1951) as modified by Lallemant (1985)]; comm.). The next step of this ongoing project is to acquire the 0.2% glucose malt-yeast extract (w/v) [0.2% G-MY; modified in fungal genome for comparison both two complete genome this study from Ahmadjian (1993) as follows: 5 g of malt (photobiont and mycobiont). Anaptychia ciliaris has been extract, 2 g of glucose, 0.25 g of yeast extract, and 15 g of agar mycoscience 56 (2015) 351e358 353 in 1 L of D.W.], and corn meal agar (CMA) following manu- and editing sequence followed protocols according to Molina facturer's instructions (Difco, Detroit, MI, USA). In parallel, we et al. (2011). The sequence were blasted against GenBank continued to study the spore development in germination database (http://www.ncbi.nlm.nih.gov/genbank/) following media (inorganic BBM and organic 1% G-BBM). Differences in the methodology outlined in Sayers et al. (2011) to approach growth rates were studied in a total of six media (two germi- the species identity as A. ciliaris. The culture reported here nation and four development media) after 50, 100, and 300 from CMA was submitted to Fungal culture Bank of Korean days.
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