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Evidence for Successional Development in Antarctic Hypolithic Bacterial Communities

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Evidence for Successional Development in Antarctic Hypolithic Bacterial Communities The ISME Journal (2013) 7, 2080–2090 & 2013 International Society for Microbial Ecology All rights reserved 1751-7362/13 www.nature.com/ismej ORIGINAL ARTICLE Evidence for successional development in Antarctic hypolithic bacterial communities Thulani P Makhalanyane1,2, Angel Valverde1,2, Nils-Ka˚re Birkeland3, Stephen C Cary4, I Marla Tuffin1 and Don A Cowan1,2 1Department of Genetics, Centre for Microbial Ecology and Genomics, University of Pretoria, Pretoria, South Africa; 2Institute for Microbial Biotechnology and Metagenomics, University of the Western Cape, Cape Town, South Africa; 3Department of Biology, Centre for Geobiology, University of Bergen, Bergen, Norway and 4Department of Biological Sciences, University of Waikato, Hamilton, New Zealand Hypoliths (cryptic microbial assemblages that develop on the undersides of translucent rocks) are significant contributors to regional C and N budgets in both hot and cold deserts. Previous studies in the Dry Valleys of Eastern Antarctica have reported three morphologically distinct hypolithic community types: cyanobacteria dominated (type I), fungus dominated (type II) and moss dominated (type III). Here we present terminal-restriction fragment length polymorphism analyses to elucidate the bacterial community structure in hypolithons and the surrounding soils. We show clear and robust distinction in bacterial composition between bulk surface soils and hypolithons. Moreover, the bacterial assemblages were similar in types II and III hypolithons and clearly distinct from those found in type I. Through 16S rRNA gene 454 pyrosequencing, we show that Proteobacteria dominated all three types of hypolithic communities. As expected, Cyanobacteria were more abundant in type I hypolithons, whereas Actinobacteria were relatively more abundant in types II and III hypolithons, and were the dominant group in soils. Using a probabilistic dissimilarity metric and random sampling, we demonstrate that deterministic processes are more important in shaping the structure of the bacterial community found in types II and III hypolithons. Most notably, the data presented in this study suggest that hypolithic bacterial communities establish via a successional model, with the type I hypolithons acting as the basal development state. The ISME Journal (2013) 7, 2080–2090; doi:10.1038/ismej.2013.94; published online 13 June 2013 Subject Category: Microbial population and community ecology Keywords: Antarctica; community assembly; hypoliths; pyrosequencing; soil; succession; T-RFLP Introduction species has been found in various niches ranging from permafrost to the ice-free arid terrestrial zones Antarctica is regarded as one of the most ‘extreme’ (Yergeau et al., 2007; Stomeo et al., 2012). environments on Earth (Cowan and Ah Tow, 2004; Hypolithic communities are widely distributed in Convey and Stevens, 2007; Cary et al., 2010). The hot (Schlesinger et al., 2003; Warren-Rhodes et al., McMurdo Dry Valleys of Eastern Antarctica are 2007; Makhalanyane et al., 2013) and cold deserts characterized by very low levels of precipitation, (Cockell and Stokes, 2004; Smith et al., 2006; episodic katabatic winds, high salt content and Wood et al., 2008; Pointing et al., 2009; Wong extremely low temperatures (Cowan and Ah Tow, et al., 2010; Khan et al., 2011). The hypolithic 2004; Cary et al., 2010). Although it has frequently ‘lifestyle’ is proposed to circumvent environmental been assumed that these extreme factors would stress as the rock provides attenuation from exces- result in both low cell numbers and species sive ultraviolet, photosynthetically active radiation, diversity, recent data have supported the view that freeze thaw events and enhanced water availability species diversity is higher than initially thought in a (Cary et al., 2010; Cowan et al., 2010b). range of Antarctic biotopes (Cowan et al., 2002; Bacterial community composition in hypoliths Aislabie et al., 2006; Smith et al., 2006; Babalola has been shown to differ from that of soil commu- et al., 2009). Evidence of potentially novel microbial nities (Pointing et al., 2009; Khan et al., 2011; Makhalanyane et al., 2013, Stomeo et al., 2013), and Correspondence: DA Cowan, Department of Genetics, Centre for to be dominated by cyanobacteria (reviewed in Chan Microbial Ecology and Genomics, University of Pretoria, Pretoria et al. (2012) and Pointing and Belnap (2012)). 0028, South Africa. Actinobacteria, Alphaproteobacteria and Gamma- E-mail: [email protected] Received 10 December 2012; revised 14 May 2013; accepted 14 proteobacteria are ubiquitous in all hypoliths May 2013; published online 13 June 2013 (Pointing et al., 2009; Wong et al., 2010), whereas Community structure and assembly in hypoliths TP Makhalanyane et al 2081 Bacteroidetes, Acidomicrobia, Verrucomicrobia, succession (Fierer et al., 2010) and stochastic Archaea, fungi or mosses represent small compo- processes predominate in higher-productivity nents (Khan et al., 2011). However, recently, two systems (Chase, 2010), we hypothesize that stochas- other hypolithic morphotypes have been described ticity will be stronger in cyanobacterial-relative to in the Antarctic Miers Valley (Cowan et al., 2010a): fungal- and moss-dominated hypolithons. type II, dominated by fungal mycelia, and type III, We used terminal-restriction fragment length dominated by bryophyte-based communities. Con- polymorphism (T-RFLP) to show that hypoliths sequently, the cyanobacteria-dominated hypoli- and soil harbor distinct bacterial communities. thons are referred as type I. In an observational We then assessed bacterial community composition study, it has been suggested that the three hypoli- using 16S rRNA gene 454 pyrosequencing. As alpha- thons may represent sequential development stages diversity varied among communities, we tested for (Cowan et al., 2010a). As Antarctic soils contain mechanisms in community assembly by means of a relatively low levels of organic carbon (Cary et al., probabilistic dissimilarity metric and random sam- 2010) the more obvious hypothesis is that photo- pling. We present evidence that species sorting is autotrophic hypolithons (type I) are the primary more important in shaping the structure of types II stage in succession. The increased eutrophication of and III relative to type I hypolithons. the hypolithic microenvironment resulting from cyanobacterial colonization could serve as a trigger for heterotrophic fungal colonization (type II; Cowan Materials and methods et al., 2010a). It was proposed that the development of the type III community may be controlled more by Sampling and soil physicochemical analysis growth kinetics and then by nutrient status, on the Samples were collected from the coastal Miers 0 0 basis that Antarctic mosses have very slow growth Valley (78160 S, 164100 E) region of Eastern rates (Fenton, 1980) in comparison to cyanobacteria. Antarctica. The surface topology of the Miers Valley Hypoliths in extreme environments may be the is composed of moraine of glacial and/or marine dominant sites of primary productivity (Tracy et al., origin (Bockheim and McLeod, 2008). A total of 36 2010), N input (Cowan et al., 2011) and the basis for samples were collected, 9 from each of the three the survival of whole ecosystems (Thomas, 2005). hypolith types and soil (that is, four habitats), and Therefore, understanding their species composition stored in sterile Whirl-Pak bags (Nasco Inter- (alpha-diversity), how they vary across sites national, Fort Atkinson, WI, USA). Equivalent (beta-diversity) and the factors and processes that amounts of hypolithic and soil samples were 2 control them is of particular relevance in desert collected aseptically in an area of 1 km with similar microbiology research. macro-environmental conditions (that is, slope, Beta-diversity varies with environmental gradi- aspect, elevation). The spatial arrangement of sam- ents (for example, productivity), environmental ples was also similar between habitats, therefore, heterogeneity and disturbance regime, and depends allowing us to compare the potential influence on dispersal or connectivity among patches (Chase, of micro-environmental factors on beta-diversity 2003, 2007, 2010). In general, beta-diversity can be across a similar spatial scale. Samples were main- influenced by local (for example, environmental tained at À 20 1C and transported to the University conditions and species interactions) and regional of the Western Cape (South Africa) and stored at (for example, demographic stochasticity and dis- À 80 1C for further analysis. persal) habitat factors (Lindstro¨m and Langenheder, The slurry technique was used to measure pH by 2012). Community assembly processes driven by mixing 2 g of soil with 5 ml of deionized water and local contemporary factors are often named niche allowing it to settle with a CRISON Bench meter based, species sorting or deterministic processes, (Crison Instruments, Barcelona, Spain). Soil chemi- whereas those driven by regional factors are cal analysis was analyzed using a LECO Truspec so-called neutral, historical or stochastic processes. Elemental Determinator at the Stellenborsch Central Recently, both deterministic and stochastic pro- Analytical Facilities (Stellenbosch University, cesses have been shown to be important in shaping SA). Sample measurements were conducted for both À À 2 À À the landscape distribution patterns of type I anions (F ,Cl,SO4 and NO3 ) and elements hypolithons (Caruso et al., 2011; Makhalanyane (%N, %C and %S), and were analyzed
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