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Edaphic Sorting Drives Arbuscular Mycorrhizal Fungal Community Assembly in a Serpentine/Non-Serpentine Mosaic Landscape 1, S

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Edaphic Sorting Drives Arbuscular Mycorrhizal Fungal Community Assembly in a Serpentine/Non-Serpentine Mosaic Landscape 1, S Edaphic sorting drives arbuscular mycorrhizal fungal community assembly in a serpentine/non-serpentine mosaic landscape 1, S. P. SCHECHTER AND T. D. BRUNS Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 USA Citation: Schechter, S. P., and T. D. Bruns. 2012. Edaphic sorting drives arbuscular mycorrhizal fungal community assembly in a serpentine/non-serpentine mosaic landscape. Ecosphere 3(5):42. http://dx.doi.org/10.1890/ES12-00059.1 Abstract. Serpentine soil generates distinct plant assemblages, but it is not known how this edaphically extreme environment affects arbuscular mycorrhizal fungal (AMF) assembly or how this may contribute to plant adaptation to serpentine. Our previous studies showed that serpentine and non-serpentine adapted ecotypes of Collinisa sparsiflora associates with distinct AMF assemblages, but a common garden experiment showed that this pattern was not due to host-fungal preference. We hypothesized that the observed differences in AMF associated with C. sparsiflora ecotypes was driven by edaphically defined AMF assemblages. To test this idea we employed a broader sampling of the plant community from five serpentine and five non-serpentine sites in close proximity (50–150 m between sites) and identified AMF and plant species associated with root samples by amplifying rDNA and cpDNA respectively, cloning, and sequencing. We compared AMF and plant assemblages, and measured the relative contribution of distance, plant and soil factors on AMF assembly. Analyses clearly showed that serpentine and non-serpentine AMF assemblages are distinct—with the complete absence of the non-serpentine dominant AMF taxon on serpentine. These results show strong edaphic sorting of serpentine tolerant/adapted AMF taxa in serpentine soil and indicate a strong ecological correlation between AMF and plant tolerance to serpentine soil. Key words: arbuscular mycorrhizal fungi (AMF); community assembly; cpDNA; ecological sorting; edaphic factors; fungal community; McLaughlin Reserve, Lake County, California, USA; plant community; rDNA; serpentine; soil type. Received 24 February 2012; accepted 6 April 2012; published 11 May 2012. Corresponding Editor: K. Elgersma. Copyright: Ó 2012 Schechter and Bruns. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits restricted use, distribution, and reproduction in any medium, provided the original author and sources are credited. 1 Present address: United States Department of Agriculture, Forest Service, Pacific Southwest Research Station, 1731 Research Park Drive, Davis, California 95618 USA. E-mail: [email protected] INTRODUCTION areas within non-serpentine soil types generating an abruptly heterogeneous landscape sometimes Serpentine soils are well known for generating at fine spatial scales (Davies et al. 2005). These distinct plant assemblages. Derived from ultra- abrupt changes in edaphic conditions pose severe mafic rock, serpentine soils are characterized by a challenges to plant growth leading to strong very low Ca:Mg ratio, low levels of essential selection of serpentine tolerant and intolerant nutrients (N, P, K), high to toxic levels of heavy species, locally adapted ecotypes, as well as metals (Fe, Cr, Co, Ni), and drought susceptibil- endemic (serpentine restricted) plant species ity (Brooks 1987, Brady et al. 2005). Serpentine (Kruckeberg 1984, Rajakaruna 2004, Brady et al. soils often occur as discontinuous ‘‘island-like’’ 2005). But very little is known about how v www.esajournals.org 1 May 2012 v Volume 3(5) v Article 42 SCHECHTER AND BRUNS serpentine edaphic factors shape assembly of (2003) described extreme edaphic habitats (e.g., important plant symbionts or what role a serpentine, heavy metal mine tailings, acid bogs) potentially serpentine tolerant/adapted symbiont as examples of environmental islands in which a assemblage may play in plant adaptation to species niche space is defined by adaptive serpentine. evolution (i.e., the ability or inability to adapt AMF are common root symbionts that can to a specific edaphic stress). For instance, metal increase their plant hosts’ establishment and contaminated sites are associated with metal- growth in stressful environments by enhancing tolerant AMF taxa (Gildon and Tinker 1981, nutrient and water uptake and may provide Weissenhorn and Leyval 1995, Gonzalez-Chavez protection against toxic conditions (Yost and Fox et al. 2002), thus variation between AMF species 1979, Habte and Manjunath 1987, Meharg 2003). in tolerance of and/or adaptation to a specific Plant adaptation to complex serpentine edaphic metal contaminant can generate differences in factors is not fully explained by plant physiolog- assemblage composition (Meharg and Cairney ical and morphological traits alone (Brady et al. 1999, Meharg 2003). 2005, Wright and Stanton 2007). Therefore, plant Serpentine soils provide an excellent system to traits (e.g., requirement for and response to study the effect of extreme edaphic factors on AMF) and fungal traits (e.g., tolerance of or AMF assemblage structure and composition. adaptation to edaphic stress) which affect the Much like the anthropogenically contaminated symbiotic functioning under nutrient and metal sites discussed above, serpentine soils often have stress have the potential to contribute to plant high concentrations of toxic metal ions, but growth and fitness in harsh serpentine edaphic unlike contaminated sites, serpentine has existed conditions. Our 2008 study (Schechter and Bruns in particular areas for 10,000 to 10 million years 2008) showed that serpentine and non-serpentine (Kruckeberg 1984) and so provide a more adapted ecotypes of Collinsia sparsiflora associat- sustained selective regime on AMF taxa. If plants ed with distinct AMF assemblages. Since we did are a good model, one would predict that the a not find evidence of AMF dispersal limitation heterogeneous serpentine habitat would serve as between C. sparsiflora ecotype locations we an ecological filter for AMF taxa as well and hypothesized that the distinction between plant generate serpentine tolerant and intolerant AMF ecotype AMF assemblages could be due to taxa, locally adapted ecotypes, and/or unique specificity between adapted plant genotypes and possibly endemic serpentine AMF. Distinct and adapted fungal genotypes within a ubiqui- serpentine adapted AMF assemblages may pro- tous AMF assemblage. However, the distinction vide specific services to plants in this harsh between the plant ecotype AMF assemblages was environment and facilitate plant adaptation to also correlated with the dissimilarity in rhizo- serpentine. However, it is difficult to isolate sphere soil chemistry associated with serpentine edaphic factors from the influence of plant and non-serpentine plant ecotypes. Thus, the community differences on AMF assemblage distinct AMF assemblages that we found associ- structure and composition (Johnson et al. 1992, ated with the two different ecotypes of C. Bever et al. 2002). We know that the extreme sparsiflora maysimplyhavebeendrivenby edaphic factors of serpentine soil generates edaphic factors rather than host genetic differ- distinct serpentine floras (Kruckeberg 1984, ences. Brady et al. 2005). Therefore, any comparison of Both niche and neutral processes play roles in serpentine and non-serpentine AMF assemblages AMF community assembly (Dumbrell et al. must also account for differences in associated 2010). Soil pH, soil texture and spatial distance plant assemblages. (as a proxy for dispersal limitation) have all been The goal of this study is to examine if there are shown to have a role in AMF assemblage edaphically distinct AMF assemblages that asso- structure and composition (Johnson et al. 1992, ciate with the broader plant communities present Lekberg et al. 2007, Dumbrell et al. 2010, Lekberg on serpentine and non-serpentine soils. This et al. 2011). Thus, heterogeneous extreme edaph- result will help explain the distinction between ic environments are also likely to generate AMF assemblages observed associating with dissimilarity in AMF assemblages. Ackerly serpentine and non-serpentine C. sparsiflora eco- v www.esajournals.org 2 May 2012 v Volume 3(5) v Article 42 SCHECHTER AND BRUNS Fig. 1. Study area at Donald and Sylvia McLaughlin Reserve, part of the University of California Davis natural reserve system in Northern California. Dots represent the research grid, labels indicate the location of serpentine (S1, S2, S3, S4, and S5) and non-serpentine (NS1, NS2, NS3, NS4, NS5) grid points sampled in this study. types at the same location (Schechter and Bruns MATERIALS AND METHODS 2008). To carry out this study, we compared AMF assemblages associated with randomly sampled Study system plant roots found in adjacent serpentine and non- This study was done at the Donald and Sylvia serpentine soil types using molecular methods. McLaughlin University of California Natural We took advantage of the fine-scale mosaic of Reserve located in Napa, Lake, and Yolo counties serpentine and non-serpentine soils associated in northern California (Fig. 1). The McLaughlin with the McLaughlin Reserve Research Grid to reserve is situated over a minor fault line that has sample serpentine and non-serpentine sites with- produced a fine-scale mosaic of serpentine, in a close geographical range (50–150 m between volcanic, and valley sediment soil types occur- sites) in order to limit the influence of dispersal ring
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