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Environmental Controls Over Bacterial Communities in Polar Desert Soils 1, 1 2 2 KEVIN M Environmental controls over bacterial communities in polar desert soils 1, 1 2 2 KEVIN M. GEYER, ADAM E. ALTRICHTER, DAVID J. VAN HORN, CRISTINA D. TAKACS-VESBACH, 3,4 1 MICHAEL N. GOOSEFF, AND J. E. BARRETT 1Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061 USA 2Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131 USA 3Department of Civil and Environmental Engineering, Pennsylvania State University, University Park, Pennsylvania 16802 USA Citation: Geyer, K. M., A. E. Altrichter, D. J. Van Horn, C. D. Takacs-Vesbach, M. N. Gooseff, and J. E. Barrett. 2013. Environmental controls over bacterial communities in polar desert soils. Ecosphere 4(10):127. http://dx.doi.org/10.1890/ ES13-00048.1 Abstract. Productivity-diversity theory has proven informative to many investigations seeking to understand drivers of spatial patterns in biotic communities and relationships between resource availability and community structure documented for a wide variety of taxa. For soil bacteria, availability of organic matter is one such resource known to influence diversity and community structure. Here we describe the influence of environmental gradients on soil bacterial communities of the McMurdo Dry Valleys, Antarctica, a model ecosystem that hosts simple, microbially-dominated foodwebs believed to be primarily structured by abiotic drivers such as water, organic matter, pH, and electrical conductivity. We sampled 48 locations exhibiting orders of magnitude ranges in primary production and soil geochemistry (pH and electrical conductivity) over local and regional scales. Our findings show that environmental gradients imposed by cryptogam productivity and regional variation in geochemistry influence the diversity and structure of soil bacterial communities. Responses of soil bacterial richness to carbon content illustrate a productivity-diversity relationship, while bacterial community structure primarily responds to soil pH and electrical conductivity. This diversity response to resource availability and a community structure response to environmental severity suggests a need for careful consideration of how microbial communities and associated functions may respond to shifting environmental conditions resulting from human activity and climate variability. Key words: Antarctic Dry Valleys; biogeography; environmental gradients; microbial ecology; productivity/diversity theory. Received 15 February 2013; revised 17 July 2013; accepted 18 July 2013; final version received 17 September 2013; published 25 October 2013. Corresponding Editor: U. Nielsen. Copyright: Ó 2013 Geyer et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. http://creativecommons.org/licenses/by/3.0/ 4 Present address: Department of Civil and Environmental Engineering, Colorado State University, Fort Collins, Colorado 80523 USA. E-mail: [email protected] INTRODUCTION ing a diverse microbial world exhibiting spatial patterns over environmental gradients spanning Despite early suggestions that microbial taxa meter, kilometer (Noguez et al. 2005, Zeglin et al. experience cosmopolitan distribution (Baas Beck- 2011) and regional to continental scales (Fierer ing 1934, Finlay 2002), recent evidence is reveal- and Jackson 2006, Yergeau et al. 2007, Bryant et v www.esajournals.org 1 October 2013 v Volume 4(10) v Article 127 GEYER ET AL. al. 2008). Although geographic patterns in soil organic matter content and extreme ranges of microbial communities are now evident, the soil pH (.9.0) and salinity (.10,000 lS/cm) mechanisms driving them remain poorly under- (Bockheim 1997). Distinct biogeochemical gradi- stood (Soininen 2012). One promising avenue for ents span orders of magnitude in nutrient beginning to frame hypotheses behind microbial availability, major ion concentrations, and bio- biogeography is the application of macroecolog- mass (Barrett et al. 2004, Poage et al. 2008), ical theory, with which researchers may test characteristics of a landscape where abiotic whether controls over the spatial organization factors are the primary controls over the diversity of eukaryotic communities are equally appropri- and structure of microbial communities. Recent ate for microorganisms (Martiny et al. 2006, research conducted in this region has described Soininen 2012). responses of microbial communities to a number Environmental controls have been long recog- of abiotic drivers including: water availability nized as major drivers of a species’ presence/ (Zeglin et al. 2011); geochemistry (Lee et al. absence and abundance (Ricklefs and Schluter 2012); carbon concentration (Aislabie et al. 2009); 1994). For instance, productivity-diversity hy- or a combination of these factors (Niederberger et potheses predict that spatial or temporal varia- al. 2008, Smith et al. 2010, Stomeo et al. 2012). tion in resource availability (e.g., nitrogen, The anticipated response of dry valley biota to organic matter) influences communities by elic- environmental controls is also supported by iting niche-specialization of, and even competi- evidence from other ecosystems and experimen- tive exclusion by, particular species across ranges tal manipulations, which have demonstrated a of nutrient availability or productivity (Tilman community response to environmental variabil- 1982, Waide et al. 1999). Often a unimodal ity, such as positive influences of moisture levels (hump-shaped curve) relationship is observed on diversity (Zhou et al. 2002) and effects on between productivity and diversity, a result of community similarity due to carbon substrate positive effects of resource availability and (resource) diversity (Orwin et al. 2006, Eilers et negative effects of competition along a gradient al. 2010). of increasing ecosystem production (Michalet et Here we focus on the distinct effects of al. 2006). Field surveys (Abramsky and Rose- resource availability on both bacterial communi- nzweig 1984, Mittelbach et al. 2001) and exper- ty diversity and structure, as well as the imental resource manipulations (Silvertown et al. influences of geochemical severity (pH and 2006, Chase 2010) support these predictions for a salinity). To evaluate these abiotic drivers we variety of taxa in terrestrial and aquatic ecosys- studied soils representing a productivity gradient while additionally capturing an extensive range tems. Environmental severity (e.g., extreme pH in geochemical conditions. Based on evidence or salinity) may also generate a range of physical from productivity/diversity theory and other conditions that influences productivity, habitat field surveys, we hypothesize: (1) bacterial suitability, and community structure of organ- community diversity will exhibit a positive isms (Freckman and Virginia 1997, Lee et al. relationship with resource availability (organic 2012). Given the universal constraints to biolog- carbon and/or water) and a negative association ical diversity and activity which arise from both with geochemical severity, while (2) bacterial resource limitations and environmental severity, community structure will be influenced by both these mechanisms likely operate together to resource availability and geochemical severity. In control macro- and microorganismal community addition we quantify a gradient of primary structure alike (Prosser 2007). Indeed, examples production (chlorophyll a) for Antarctic soils of significant productivity/diversity relationships and examine the influence of aboveground have been reported for microorganisms (Horner- productivity on belowground biology and bio- Devine et al. 2003, Smith 2007, Logue et al. 2012). geochemistry. Antarctica’s polar deserts are a model system in which to address questions of controls over microbial biogeography. Resident organisms are sensitive to resource availability, and abiotic factors in general, given the exceptionally low v www.esajournals.org 2 October 2013 v Volume 4(10) v Article 127 GEYER ET AL. Fig. 1. Location of sixteen regional sampling sites in Wright and Taylor Valley of the McMurdo Dry Valleys, Antarctica. See Table 1 for an explanation of site labels. METHODS ents (Barrett et al. 2009) and promoting localized hotspots of primary production (Barrett et al. Site description 2006). The McMurdo Dry Valleys are an ice-free polar The soil food web is simple, microbially- desert in Southern Victoria Land, Antarctica. dominated, and at the base composed of various Aridity (generally less than 10cm of annual prokaryotic, photosynthetic bacteria (Families precipitation), temperature (mean annual be- Nostocaceae, Oscillatoriaceae), eukaryotic algae tween À168CtoÀ218C), and low soil organic carbon availability (0.03% average by weight) (Phyla Chlorophyta, Bacillariophyta), and fewer together constrain the diversity and activity of than 10 species of moss (Family Bryaceae) native biota (Kennedy 1993, Burkins et al. 2000, (Broady 1996, Seppelt and Green 1998) that Hogg et al. 2006). Dry permafrost soils are poorly associate in cryptogamic communities. Several weathered and composed of .90% sand-sized species each of tardigrades, rotifers, and nema- particles with ice cement occurring within 0.5 m todes represent the apex of the soil foodweb of the surface (Ugolini and Bockheim 2008). (Freckman and Virginia 1997, Adams et al. 2006). Salinity and pH are generally
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