FEMS Microbiology Ecology, 94, 2018, fiy129 doi: 10.1093/femsec/fiy129 Advance Access Publication Date: 30 June 2018 Research Article RESEARCH ARTICLE Microbial distribution and turnover in Antarctic Downloaded from https://academic.oup.com/femsec/article-abstract/94/9/fiy129/5047302 by guest on 09 March 2020 microbial mats highlight the relevance of heterotrophic bacteria in low-nutrient environments Patricia M. Valdespino-Castillo1, Daniel Cerqueda-Garc´ıa2,Ana Cecilia Espinosa3, Silvia Batista1,Mart´ın Merino-Ibarra4, Neslihan Tas¸ 5, Roc´ıo J. Alcantara-Hern´ andez´ 6 and Luisa I. Falcon´ 2,* 1Unidad de Microbiolog´ıa Molecular, Instituto de Investigaciones Biologicas´ Clemente Estable, Montevideo, 11600, Uruguay, 2Laboratorio de Ecolog´ıa Bacteriana, Instituto de Ecolog´ıa, Universidad Nacional Autonoma´ de Mexico,´ CDMX, 04510, Mexico, 3LANCIS, Instituto de Ecolog´ıa, Universidad Nacional Autonoma´ de Mexico,´ CDMX, 04510, Mexico, 4Unidad Academica´ de Ecolog´ıa y Biodiversidad Acuatica,´ Instituto de Ciencias del Mar y Limnolog´ıa, Universidad Nacional Autonoma´ de Mexico,´ CDMX, 04510, Mexico, 5Earth and Environmental Sciences Area, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, US and 6Instituto de Geolog´ıa, Universidad Nacional Autonoma´ de Mexico,´ CDMX, 04510, Mexico ∗Corresponding author: Instituto de Ecolog´ıa, Universidad Nacional Autonoma´ de Mexico.´ Circuito exterior sn, Cd. Universitaria, Coyoacan,´ 04510, Mexico.´ Tel: +52-55-56228222; E-mail: [email protected] + − One sentence summary: Maritime Antarctica inland microbial mat community structure is explained by environmental NH4 ,NO3 , DIN, soluble reactive silicon and conductivity. Editor: Carsten Jacobsen ABSTRACT Maritime Antarctica has shown the highest increase in temperature in the Southern Hemisphere. Under this scenario, biogeochemical cycles may be altered, resulting in rapid environmental change for Antarctic biota. Microbes that drive biogeochemical cycles often form biofilms or microbial mats in continental meltwater environments. Limnetic microbial mats from the Fildes Peninsula were studied using high-throughput 16S rRNA gene sequencing. Mat samples were collected from 15 meltwater stream sites, comprising a natural gradient from ultraoligotrophic glacier flows to meltwater streams exposed to anthropogenic activities. Our analyses show that microbial community structure differences between mats are + − explained by environmental NH4 ,NO3 , DIN, soluble reactive silicon and conductivity. Microbial mats living under ultraoligotrophic meltwater conditions did not exhibit a dominance of cyanobacterial photoautotrophs, as has been documented for other Antarctic limnetic microbial mats. Instead, ultraoligotrophic mat communities were characterized by the presence of microbes recognized as heterotrophs and photoheterotrophs. This suggests that microbial capabilities for recycling organic matter may be a key factor to dwell in ultra-low nutrient conditions. Our analyses show that phylotype level assemblages exhibit coupled distribution patterns in environmental oligotrophic inland waters. The evaluation of Received: 29 November 2017; Accepted: 4 June 2018 C FEMS 2018. All rights reserved. For permissions, please e-mail: [email protected] 1 2 FEMS Microbiology Ecology, 2018, Vol. 94, No. 9 these microbes suggests the relevance of reproductive and structural strategies to pioneer these psychrophilic ultraoligotrophic environments. Keywords: microbial mats; ultraoligotrophy; photoheterotrophs; psychrophilic; Antarctica INTRODUCTION Fernandez-Valiente´ et al. 2007; Callejas et al. 2011; Cameron, Hod- son and Osborn 2012a,b;Smithet al. 2016) although the relation- Polar regions have shown significant ice decline as a conse- ships with environmental parameters, particularly at the phylo- quence of global climate change (Schmidtko et al. 2014). Further- type level need further exploration. The aim of this study was to more, in some areas of Maritime Antarctica, the rise of approx- delineate the identity and turnover of extreme oligotrophs and imately 3◦C in the last 50 years represents the highest relative how environmental parameters may influence the microbial increase in temperature in the Southern Hemisphere (Turner, Downloaded from https://academic.oup.com/femsec/article-abstract/94/9/fiy129/5047302 by guest on 09 March 2020 community structure in inland Antarctica. We compared micro- Overland and Walsh 2007; Sahade et al. 2015). The changing con- bial mats on the Fildes Peninsula found in a natural gradi- ditions of natural habitats are likely to have an impact on native ent from ultraoligotrophic glacier flows to ice-melt streams biota, affecting organism-to-community structure, function, fit- exposed to anthropogenic activities. The patterns and turnover ness and diversity. of microbes along environmental gradients studied here can Among psychrophilic biota, limnetic microbial mats harbor help to understand community function (such as colonization) a large fraction of biomass in extreme environments including and assess functional redundancy within the mat´s interacting inland Antarctica (Quesada et al. 2008). Antarctic microbial mats taxa. are fundamental players in key ecosystem processes such as primary production and biogeochemical cycling (Vincent 2000; Quesada et al. 2008;Alcantara-Hern´ andez´ et al. 2014). Assem- blages of inland psychrophilic microorganisms face extreme conditions that include low temperature and water scarcity METHODS short growing seasons (mainly during the Austral summer) and low-light intensity regimes, freeze-thaw cycles (Davey 1989), Sample collection high salinity (in Antarctic lakes, Bowman et al. 2000), high The spring and summer temperatures in Maritime Antarctica heavy metal concentrations (Osyczka, Dutkiewicz and Olech create an inland landscape where water ponds as well as snow 2007; Padeiro et al. 2016), high UV radiation, low conductivity and and ice-melt streams are abundant. Melting of winter ice is low nutrient availability (Copes et al. 1997; Toro et al. 2007;Mar- abrupt, but soon thereafter, water flow is reduced and streams gesin and Miteva 2011). To thrive under such extreme environ- and ponds harbor water with longer residence times. Ponds and mental conditions, microorganisms exhibit diverse (structural, streams continuously freeze and thaw during these months; metabolic) strategies to survive, e.g. pigments adapted to ultra- some streams and ponds have the same location year after year violet irradiance, carbon and nitrogen cycling genetic potential, (dictated by geographical features; e.g. proximity to ice caps) complex organic compounds degradation capabilities through and others occur in association with spring-summer precipi- low-temperature enzymatic performance (Bowman et al. 2000; tation. Microbial mats occur in these environments (seasonal Quesada et al. 2008; Cameron, Hodson and Osborn 2012b; Loper- melting systems, usually at depths of ∼ 0.1 m), over rocks or ena et al. 2012;Alcantara-Hern´ andez´ et al. 2014;Lav´ın et al. 2016). sediment (e.g., inland Fildes Peninsula, Fig. 1). Sampling areas The frequency and distribution patterns of microorganisms included three North-South transects on the Fildes Peninsula in environmental gradients contribute to ecological theory, and from the Western tip of the Peninsula to the edge of the mas- particularly to understand, and possibly to predict, changes in a sive Bellingshausen Glacier (Fig. 1) during the Austral summer community structure in response to environmental change (Gra- (February) of 2014. The presence of ice-melt streams and micro- ham and Fine 2008). When considering ultraoligotrophic envi- bial mats determined specific collection sites (Fig. 1)alongthe ronments, distribution patterns or microbial assemblage rules Fildes Peninsula (Western King George Island, Maritime Antarc- (if any) might reveal the conditions affecting microbial composi- tica); some sites were in remote (protected) areas, while others tion over successional time, or in response to rapid environmen- were in proximity to locations with higher anthropogenic pres- tal change. Trophic status of freshwater ecosystems might be ence. This region, which includes Maritime Antarctica and the significantly affected under scenarios of global change; i.e. phos- North of the Antarctic Peninsula, has been identified as one of phorus loading in temperate and polar freshwater environments the regions with the highest warming rates on earth (i.e., tem- is expected to be enhanced as a consequence of global warming perature increase at a rate of 0.56 ◦C per decade; and a winter (Arctic Climate Impact Assessment 2002; (IPCC and Watson et trend of 1.09 ◦C per decade in the Western side of the Antarctic al. 2001) and increased nitrogen deposition is also predicted as Peninsula; Turner, Overland and Walsh 2007). a consequence of present and future human activity (Vitousek Sampling sites at the Western-end of the Peninsula include et al. 1997). These changes in cycling of the main biogeochemical (AE.1-2), sites in the central part of the peninsula include (ACB.1- elements may promote increasing emergent problems in natu- 2), and sites in closer proximity to the Bellingshausen Glacier ral systems such as eutrophication (Jeppesen et al. 2009)orbio- edge include (AD.1-6 and GCB.1-4) (Fig. 1). Microbial mat sam- logical invasions (Dukes and Mooney 1999) among other ecosys- pling sites were separated from one another by at least 400 m; temic processes. therefore,