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The Extremophile Endolithella Mcmurdoensis Gen. Et Sp. Nov J. Phycol. 56, 208–216 (2020) © 2019 Phycological Society of America DOI: 10.1111/jpy.12940 THE EXTREMOPHILE ENDOLITHELLA MCMURDOENSIS GEN. ET SP. NOV. (TREBOUXIOPHYCEAE, CHLORELLACEAE), A NEW CHLORELLA-LIKE ENDOLITHIC ALGA FROM ANTARCTICA1 Teresa P. Martins4, Vitor Ramos2,4 , Guilherme S. Hentschke, Raquel Castelo-Branco4, Adriana Rego Centro Interdisciplinar de Investigacß~ao Marinha e Ambiental, Universidade do Porto, Terminal de Cruzeiros do Porto de Leixoes,~ 4450-208 Matosinhos, Portugal Maria Monteiro Centro Interdisciplinar de Investigacß~ao Marinha e Ambiental, Universidade do Porto, Terminal de Cruzeiros do Porto de Leixoes,~ 4450-208 Matosinhos, Portugal School of Science, University of Waikato, Hamilton, New Zealand ^ Angela Brito Instituto de Investigacß~ao e Inovacß~ao em Saude, Universidade do Porto, Rua Alfredo Allen 208, 4200-135 Porto, Portugal Instituto de Biologia Molecular e Celular, Universidade do Porto, Rua Alfredo Allen 208, 4200-135 Porto, Portugal Paula Tamagnini Instituto de Investigacß~ao e Inovacß~ao em Saude, Universidade do Porto, Rua Alfredo Allen 208, 4200-135 Porto, Portugal Instituto de Biologia Molecular e Celular, Universidade do Porto, Rua Alfredo Allen 208, 4200-135 Porto, Portugal Faculdade de Ciencias,^ Universidade do Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal S. Craig Cary School of Science, University of Waikato, Hamilton, New Zealand International Centre for Terrestrial Antarctic Research, University of Waikato, Hamilton, New Zealand Vitor Vasconcelos Centro Interdisciplinar de Investigacß~ao Marinha e Ambiental, Universidade do Porto, Terminal de Cruzeiros do Porto de Leixoes,~ 4450-208 Matosinhos, Portugal Faculdade de Ciencias,^ Universidade do Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal Lothar Krienitz Department of Experimental Limnology, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, D-16775 Stechlin, Germany Catarina Magalhaes~ Centro Interdisciplinar de Investigacß~ao Marinha e Ambiental, Universidade do Porto, Terminal de Cruzeiros do Porto de Leixoes,~ 4450-208 Matosinhos, Portugal Faculdade de Ciencias,^ Universidade do Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal and Pedro N. Leao~ 3 Centro Interdisciplinar de Investigacß~ao Marinha e Ambiental, Universidade do Porto, Terminal de Cruzeiros do Porto de Leixoes,~ 4450-208 Matosinhos, Portugal The McMurdo Dry Valleys constitute the largest temperatures, dry and poor soils and katabatic ice-free region of Antarctica and one of the most winds, some microbes are able to take advantage of extreme deserts on Earth. Despite the low endolithic microenvironments, inhabiting the pore 1Received 10 May 2019. Revised 20 September 2019. First Published Online 23 October 2019. Published Online 17 November 2019, Wiley Online Library (wileyonlinelibrary.com). 2Centro de Investigacß~ao de Montanha (CIMO), Instituto Politecnico de Bragancßa, Campus de Santa Apolonia, 5300-253, Bragancßa Portugal. 3Author for correspondence: e-mail [email protected]. 4These authors contributed equally to this work. Editorial Responsibility: H. Verbruggen (Associate Editor) 208 ENDOLITHELLA MCMURDOENSIS GEN. ET SP. NOV. 209 spaces of soil and constituting photosynthesis-based radiation and desiccation providing milder microcli- communities. We isolated a green microalga, mate conditions that ease the growth of microbial life Endolithella mcmurdoensis gen. et sp. nov, from an (Pointing et al. 2009) with significant diversity (Wood endolithic sandstone sample collected in the et al. 2008). In fact, some microbes are able to inha- McMurdo Dry Valleys (Victoria Land, East bit porous rocks such as sandstones (Friedmann Antarctica) during the K020 expedition, in January 1982, Hughes and Lawley 2003), constituting photo- 2013. The single non-axenic isolate (E. mcmurdoensis synthesis-based endolithic communities (Friedmann LEGE Z-009) exhibits cup-shaped chloroplasts, and Ocampo 1976) that rely heavily on cyanobacteria electron-dense bodies, and polyphosphate granules and microalgae. In Antarctic land environments, but our analysis did not reveal any diagnostic green algae, especially Chlorella-like forms, are partic- morphological characters. On the basis of ularly abundant and diverse (Hodac et al. 2016) and phylogenetic analysis of the 18S rRNA (SSU) gene, have an important role in nutrient cycling and as pri- the isolate was found to represent a new genus mary producers, providing organic matter in the olig- within the family Chlorellaceae. otrophic soils (Tscherko et al. 2003). Herein, we describe the new trebouxiophycean Key index words: 18S rRNA; extremophiles; genus; microalga Endolithella mcmurdoensis gen. et sp. nov, LEGEcc; microalgae; sandstone isolated from an endolithic habitat in the McMurdo 0 Abbreviations: BI, Bayesian inference; DAPI, 4 ,6-dia- Dry Valleys, Antarctica, that was found by pyrose- midino-2-phenylindole; LEGEcc, Blue Biotechnology quencing analysis to be dominated by cyanobacteria. and Ecotoxicology culture collection; OTU, opera- tional taxonomic unit; QIIME, Quantitative insights into microbial ecology MATERIALS AND METHODS Sampling, isolation, and culturing. Endolithic samples (Fig. 1, A and B) were collected during the K020 Mission, that The remarkable diversity of green algae reflects a took place in January 2013, on Victoria Valley, located in great adaptive capacity, allowing for survival in the McMurdo Dry Valleys region, in South Victoria Land, Antarc- most extreme environments on Earth such as mar- tica (77°20.502 S, 161°39.306 E). Collected samples were pre- ine deep waters (Zechman et al. 2010, Hodac et al. served at À80°C in LifeGuard Solution (Mo Bio Laboratories, 2016, Spalding et al. 2016), deserts (Friedmann and Carlsbad, CA, USA). Isolate LEGE Z-009 was obtained from an Ocampo 1976, Lewis and Lewis 2005), hypersaline isolation process originally intended for isolating cyanobacte- ria (Rego et al. 2019). An aliquot of the endolithic sample was habitats (Vinogradova and Darienko 2008), or habi- washed and centrifuged three times (4500g, 3 min) with nitro- tats with temperatures below freezing point (Mor- gen-free BG110 medium (Rippka 1988). It was then inoculated gan-Kiss et al. 2008). Even in these extreme settings, into a 100 mL Erlenmeyer flask with liquid Z8 medium (Kotai green microalgae play an important ecological role 1972) as an initial enrichment culture and placed at 19°C, À2 À1 (Lyon and Mock 2014), but their diversity is far under a 12:12 h light (25 lmol photons Á m Á s ): dark from being understood, especially in unexplored cycle. When visible growth was detected, an aliquot was trans- ferred and streaked onto a solid BG110 medium plate (1.5% polar environments (Hodac et al. 2016). The life- agar supplemented with 25 lL of cycloheximide), and placed limiting environmental conditions that occur in at 12°C. Single colonies were then microscopically inspected, Antarctica are triggers for speciation and develop- selected, and re-streaked aseptically in the same medium and/ ment of endemic species, making this a particularly or in Z8, until isolation was achieved. The isolated strain was promising location for the exploration of microbial deposited in the LEGE Culture Collection in CIIMAR, and is ° ° diversity (Vincent 2000). maintained cryopreserved and at 12 C and 19 C, in liquid Z8 In Antarctica, trebouxiophycean microalgae have medium, under the identification LEGE Z-009. Pyrosequencing (16S rRNA-based) analysis of the endolithic com- been known since the description of Chlorella antarc- munity. Environmental DNA (eDNA) was extracted from the tica (Wille 1928), and many studies have highlighted same Victoria Valley sample used for isolation of the micro- the considerable diversity of this group in cold envi- alga strain, using a modification of the CTAB extraction pro- ronments (Friedmann and Ocampo 1976, Friedmann tocol (Barrett et al. 2006). The 16S small subunit (SSU) 1982, Carvalho et al. 2017, Nedbalova et al. 2017). rRNA gene was initially amplified by PCR using the universal The McMurdo Dry Valleys constitute the largest ice- primer pair 27F/1492R (Weisburg et al. 1991) and then sequenced by pyrosequencing technology. Briefly, the 16S free region of Antarctica (Horowitz et al. 1972) and rRNA gene was amplified for the V3/V4 hypervariable region one of the world’s most extreme deserts. The average with barcoded fusion primers containing the Roche-454 A annual temperature is about À22°C, winter tempera- and B Titanium sequencing adapters, an eight-base barcode tures typically of À60°C, precipitation levels are lower sequence, the forward (50-ACTCCTACGGGAGGCAG-30) and 0 0 than 100 mm water equivalent, the land is battered reverse (5 -TACNVRRGTHTCTAATYC-3 ) primers (Wang and by katabatic winds and intense UV radiation, and the Qian 2009). Amplicons were quantified by fluorimetry with soils are poor, with low levels of carbon, nitrogen, PicoGreen (Invitrogen), pooled at equimolar concentrations and sequenced in the A direction with GS 454 FLX Titanium and small amounts of clay (Wynnwilliams 1990, Ugo- chemistry, according to the manufacturer’s instructions (454 lini and Bockheim 2008, Cary et al. 2010). Despite all Life Sciences, Roche, Basel, Switzerland) at Biocant (Cantan- these extreme conditions, life exists. Soil and rocks hede, Portugal). The 454-machine-generated FASTA (.fna) act as refuges, protecting life from intense solar and quality score (.qual) files were processed using the 210 TERESA P. MARTINS ET AL. FIG. 1. (A,B) Colonization of the cryptoendolith-bearing
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