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Variation in Coastal Antarctic Microbial Community Composition at Sub-Mesoscale: Spatial Distance Or Environmental Fltering?

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Variation in Coastal Antarctic Microbial Community Composition at Sub-Mesoscale: Spatial Distance Or Environmental Fltering? FEMS Microbiology Ecology,92,2016,fw088 doi: 10.1093/femsec/fw088 Advance Access Publication Date: 27 April 2016 Research Article RESEARCH ARTICLE Variation in coastal Antarctic microbial community composition at sub-mesoscale: spatial distance or environmental fltering? Mario Moreno-Pino1, Rodrigo De la Iglesia2,3,NelsonValdivia4,5, Downloaded from Carlos Henr´ıquez-Castilo2,3,6, Alexander Galan´ 7, Beatriz D´ıez2,8 1, and Nicole Trefault ∗ 1Center for Genomics and Bioinformatics, Faculty of Sciences, Universidad Mayor, Camino La Piramide´ 5750, http://femsec.oxfordjournals.org/ Santiago 8580745 Chile, 2Department of Molecular Genetics and Microbiology, Pontifcia Universidad Catolica´ de Chile, Alameda 340, Santiago 8331150, Chile, 3Millennium Institute of Ocenography. Cabina 7, Barrio Universitario s/n, Concepcion´ 4030000, Chile, 4Instituto de Ciencias Marinas y Limnologicas,´ Facultad de Ciencias, Universidad Austral de Chile, Campus Isla Teja, Valdivia 5090000, Chile,, 5Centro de Investigacion´ FONDAP: Dinamica´ de Ecosistemas Marinos de Altas Latitudes (IDEAL), Campus Isla Teja, Valdivia 5090000, Chile, 6Department of Oceanography, Universidad de Concepcion,´ Cabina 7, Barrio Universitario s/n, Concepcion´ 4030000, Chile, 7CREA – Centro Regional de Estudios Ambientales, Universidad Catolica´ de la 8 Sant´ısima Concepcion,´ Av. Colon´ 2766, Talcahuano 4270789, Chile and Center for Climate and Resilience by guest on June 9, 2016 Research (CR)2, Blanco Encalada 22002, Santiago 8370449, Chile ∗Corresponding author: Center for Genomics and Bioinformatics, Faculty of Sciences, Universidad Mayor, Camino La Piramide´ 5750, Huechuraba, Santiago 8580745, Chile. Tel: 56-2-25189205; E-mail: [email protected] + One sentence summary: Coastal Antarctic photosynthetic eukaryote and bacterial communities respond differentially to environmental fltering at submesoscale. Editor: Josef Elster ABSTRACT Spatial environmental heterogeneity infuences diversity of organisms at different scales. Environmental fltering suggests that local environmental conditions provide habitat-specifc scenarios for niche requirements, ultimately determining the composition of local communities. In this work, we analyze the spatial variation of microbial communities across environmental gradients of sea surface temperature, salinity and photosynthetically active radiation and spatial distance in Fildes Bay, King George Island, Antarctica. We hypothesize that environmental flters are the main control of the spatial variation of these communities. Thus, strong relationships between community composition and environmental variation and weak relationships between community composition and spatial distance are expected. Combining physical characterization of the water column, cell counts by fow cytometry, small ribosomal subunit genes fngerprinting and next generation sequencing, we contrast the abundance and composition of photosynthetic eukaryotes and heterotrophic bacterial local communities at a submesoscale. Our results indicate that the strength of the environmental controls differed markedly between eukaryotes and bacterial communities. Whereas eukaryotic photosynthetic assemblages responded Received: 1November2015;Accepted: 22 April 2016 C ⃝ FEMS 2016. All rights reserved. For permissions, please e-mail: [email protected] 1 2 FEMS Microbiology Ecology,2016,Vol.92,No.7 weakly to environmental variability, bacteria respond promptly to fne-scale environmental changes in this polar marine system. Keywords: spatial variation; Antarctica; microbial community; environmental fltering; submesoscale; community composition INTRODUCTION multaneously toward a comprehensive understanding of com- munity regulation. Understanding the extent to which spatial environmental het- While the vast majority of polar marine studies on spatial erogeneity infuences diversity of organisms at different scales variation of microbial communities have focused on the bacte- is a key question in community ecology (Hanson et al. 2012; rial (e.g. Ghiglione et al. 2012; Winter, Matthews and Suttle 2013) Sutherland et al. 2013). One of the mechanisms proposed to or the eukaryote component (D´ıez et al. 2004;Jianget al. 2014; explain such infuence is environmental fltering, by which Lee et al. 2014)justfewhaveanalyzedbothmicrobialcompo- different species can co-occur based on shared tolerances or re- nents in the same analysis (Luria, Ducklow and Amaral-Zettler quirements on a particular environment. Polar systems are par- 2014). Antarctic marine waters are dominated by two key mi- ticularly interesting to test this type of processes, since global Downloaded from crobial functional groups: a well-known bacterial component, in change effects, such as rise in temperatures, melting ice and which photosynthetic bacteria are considered absent, and a less increased sea level, are occurring faster than in other sites studied photosynthetic eukaryote group, responsible for fueling of the planet (Clarke et al. 2007). In Antarctica, due to its re- marine trophic networks (reviewed in De la Iglesia and Trefault sponses to global change and a high environmental heterogene- 2012 and Wilkins et al. 2013). Antarctic bacterioplankton assem- ity caused by climate disturbances, strong environmental gra- blages are dominated by Alphaproteobacteria, specifcally by the dients at small spatial scales—like in coastal lagoons and small http://femsec.oxfordjournals.org/ worldwide-distributed SAR11 clade, and by Gammaproteobac- bays—can be observed. This fne-scale environmental variability teria, represented by SAR86 clade, member of the Oceanospiril- has been suggested to infuence Antarctic biodiversity of mac- lales order (Lopez-Garc´ ´ıa et al. 2001; Piquet et al. 2011;Grzym- robial (e.g. Valdivia et al. 2014) and microbial communities (e.g. ski et al. 2012). In the photosynthetic eukaryote group, a pre- Webster and Negri 2006; Verleyen et al. 2010). vailing trend observed is that diatoms such as Thalassiosira spp. Marine microorganisms play central roles in all marine bio- and Chaetoceros spp. generally dominate during the development geochemical process (Karl and Proctor 2007;Falkowski,Fenchel of stratifed conditions, while fagellates such as Cryptomonas and Delong 2008). They infuence climate mainly through the sp. and Phaeocystis antarctica, dominate in deeply mixed waters cycling of climate-active gases (carbon dioxide, methane, ni- (Arrigo et al. 1999). trous oxide and dimethyl sulfde) (Singh et al. 2010;Mohapatra While bacteria are capable of tolerating a wide range of envi- et al. 2013), are responsible of nearly half of the carbon fxed on by guest on June 9, 2016 ronmental forcing, such as temperature, pH, DOM, POM, salinity the planet (Behrenfeld et al. 2001), and structure healthy and and nutrients (Azam and Malfatti 2007), photosynthetic eukary- stressed marine ecosystems (Azam and Worden 2004). Hence, otes are strongly affected by light and temperature (Ardyna et al. determining the role of environmental fltering in structuring 2011;Monieret al. 2014). In Antarctic shores and bays, glacier microbial Antarctic communities will improve our predictions of melting and animal settlements signifcantly affect salinity (wa- the functional response of marine ecosystems to environmental ter density), light penetration and nutrient inputs into the wa- changes. ter column (Dierssen, Smith and Vernet 2002;Sailleyet al. 2013), The metacommunity framework explicitly incorporates the which can differentially affect the bacterial and photosynthetic effect of environmental fltering—in addition to dispersal and eukaryote components of the microbial marine community species interactions—on the structure and composition of lo- (Piquet et al. 2011). Fildes Bay (also known as Maxwell Bay) is lo- cal communities (Holyoak, Leibold and Holt 2005; Logue et al. cated between the southwest part and northeast margins of the 2011). This environmental fltering or species sorting perspective Nelson and King George Islands, respectively (Fig. 1). The hydro- is similar to the Baas-Becking hypothesis (Baas-Becking 1934) for graphic conditions of the bay are mainly modulated by freshwa- microbial communities and suggests that local environmental ter inputs from thawed drifting icebergs and from the bordering conditions provide habitat-specifc scenarios for niche require- ice caps in Fildes Peninsula and Nelson Island (Chang et al. 1990; ments, ultimately determining the composition of local com- Yoon et al. 1998). Besides, this area is particularly interesting be- munities. Therefore, dispersal among habitats should be high cause it harbors several scientifc stations with high associated enough to allow species to fll niches in habitat patches (Holyoak, anthropogenic impacts on the marine environment (Martins Leibold and Holt 2005). Considering that the major dispersal et al. 2004; Santos et al. 2005). In addition, the Collins Glacier and vehicle of microorganisms in the ocean is water-mass move- animal settlements in Nelson Island generate strong impacts in ment, it can be suggested that dispersal potential of microbial the surrounding area. All these characteristics can generate a communities might be quite high. Recent observations in sub- mosaic of environmental patches, making Fildes Bay an excel- polar and Arctic waters indicate that environmental fltering lent scenario for testing local-scale spatial phenomena and en- explains some, but not all, components of the microbial commu- vironmental fltering effect over
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