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Genuswide Acid Tolerance Accounts for the Biogeographical Distribution of Soil Burkholderia Populations

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Genuswide Acid Tolerance Accounts for the Biogeographical Distribution of Soil Burkholderia Populations bs_bs_banner Environmental Microbiology (2014) 16(6), 1503–1512 doi:10.1111/1462-2920.12211 Genus-wide acid tolerance accounts for the biogeographical distribution of soil Burkholderia populations Nejc Stopnisek,1,5 Natacha Bodenhausen,2 of the genus Burkholderia. Our results provide a Beat Frey,3 Noah Fierer,4 Leo Eberl1 and basis for building a predictive understanding of the Laure Weisskopf1,5* biogeographical patterns exhibited by Burkholderia 1Institute of Plant Biology, University of Zurich, Zürich sp. CH-8008, Switzerland. 2Institute of Microbiology, Swiss Federal Institute of Introduction Technology, Zürich CH-8093, Switzerland. 3Snow and Landscape Research, Swiss Federal The genus Burkholderia, which belongs to the β Institute for Forest, Birmensdorf CH-8903, Switzerland. -Proteobacteria class, currently comprises more than 60 4Department of Ecology and Evolutionary Biology, species that are widely distributed and frequently isolated University of Colorado, Boulder, CO 80309-0216, USA. from a large range of natural and clinical environments 5Swiss Federal Research Station for Agronomy and (Compant et al., 2008). The genus Burkholderia can be Nature, Agroscope Reckenholz-Tänikon, Zürich divided phylogenetically into two main clusters: the first CH-8046, Switzerland. one consists mainly of human, animal and plant patho- gens, e.g. the Burkholderia cepacia complex (Bcc) and the rice pathogen B. glumae. However, it is important to Summary note that some strains belonging to Bcc, such as Bacteria belonging to the genus Burkholderia are B. ambifaria or B. lata, also show plant growth-promoting highly versatile with respect to their ecological niches abilities as well as biocontrol activities against and lifestyles, ranging from nodulating tropical plants phytopathogenic fungi. The other cluster consists mainly to causing melioidosis and fatal infections in cystic of plant-beneficial-environmental (PBE) Burkholderia fibrosis patients. Despite the clinical importance and species (Suárez-Moreno et al., 2012). The members of agronomical relevance of Burkholderia species, infor- the first cluster have been extensively studied because of mation about the factors influencing their occurrence, their medical importance, but recently the PBE cluster has abundance and diversity in the environment is been the focus of research efforts with the discovery that scarce. Recent findings have demonstrated that pH is various species of this cluster are able to fix nitrogen the main predictor of soil bacterial diversity and com- (Estrada-De Los Santos et al., 2001; Martínez-Aguilar munity structure, with the highest diversity observed et al., 2008) and to nodulate legumes (Moulin et al., in neutral pH soils. As many Burkholderia species 2001). Burkholderia from the PBE cluster have been have been isolated from low pH environments, we mainly isolated from plant rhizosphere, but they are also hypothesized that acid tolerance may be a general frequently detected in sediment and bulk soil (Salles feature of this genus, and pH a good predictor of their et al., 2002; Lazzaro et al., 2008; Lim et al., 2008; Lepleux occurrence in soils. Using a combination of environ- et al., 2012; Štursová et al., 2012). In addition to their mental surveys at trans-continental and local scales, nitrogen-fixing and nodulating abilities, their versatile as well as in vitro assays, we show that, unlike most metabolism also enables them to survive in harsh condi- bacteria, Burkholderia species have a competitive tions, such as nutrient-limited or polluted environments, advantage in acidic soils, but are outcompeted in and to degrade recalcitrant compounds (Pérez-Pantoja alkaline soils. Physiological assays and diversity et al., 2012). As such, they have been suggested as good analysis based on 16S rRNA clone libraries demon- candidates for use in biotechnology, e.g. for bio- or strate that pH tolerance is a general phenotypic trait phytoremediation, biocontrol and biofertilization. Despite the high relevance of the Burkholderia genus for human health, agronomy and biotechnology, surprisingly little is Received 17 May, 2013; revised 4 July, 2013; accepted 10 July, 2013. *For correspondence. E-mail [email protected]; known about the factors underlying their geographical Tel. (+41) 44 377 72 11; Fax (+41) 44 377 72 01. distribution. © 2013 Society for Applied Microbiology and John Wiley & Sons Ltd 1504 N. Stopnisek et al. A was high (8.7), the isolated strains were all able to grow at low pH (4.5). These reports provide anecdotal evidence that Burkholderia might be tolerant to low pH conditions, which enables members of this genus to thrive in niches where others would be inhibited. We, therefore, hypoth- esized (i) that low pH tolerance is an intrinsic phenotypic trait of the Burkholderia genus, and (ii) that the relative abundance and diversity of Burkholderia populations are highest in low pH soils, with the biogeography of Burkholderia predictable from soil pH. To test these pH scale Relative abundance (%) 3 − 4 6.70 hypotheses, we developed a novel quantitative polymer- 4 − 5 5 − 6 2.82 6 − 7 ase chain reaction (qPCR) protocol to analyze the relative 1.08 7 − 8 0.01 8 − 9 0.00 abundance of Burkholderia populations in soils at a trans- B continental and a local scale. Intrageneric diversity and community structure were determined by 16S rRNA- based clone libraries constructed from a selected subset 0 20406080 200 123456 − Relative abundance (%) abundance Relative 0 of the trans-continental scale soil samples. In addition, in 45678 pH vitro physiological assays were used to test the direct −160 −140 −120 −100 −80 −60 −40 effects of pH on Burkholderia species. Fig. 1. Relative abundance of Burkholderia 16S rRNA genes in 44 Results soils. A. Representation of Burkholderia 16S rRNA gene relative Low pH tolerance, a genus-wide property of abundance at the different sites as assessed by qPCR. Relative abundance is represented by the circle size; the colour indicates Burkholderia that largely accounts for its relative the pH of the sampled soils. abundance in soils B. Influence of pH on the relative abundance of Burkholderia 16S rRNA genes. Circles represent the average of three replicates for To test whether the occurrence of Burkholderia species in each soil sample. acidic environments reflects an intrinsic capacity of this genus to tolerate low pH conditions, we tested the ability Soil pH has frequently been shown to be the main of 68 strains of Burkholderia belonging to 31 different predictor of overall soil bacterial community composition, species to grow at a pH range of 3.5–8. All Burkholderia diversity and the relative abundance of many individual strains that were tested in physiological assays grew in taxa (Tiedje et al., 1999; Fierer and Jackson, 2006; Rousk pH as low as pH 4.5. Out of 68 tested strains (31 different et al., 2010; Griffiths et al., 2011). Although it is not known species), 32 (18 species) were growing also at pH 4 and if Burkholderia distributions are related to soil pH, most 15 (8 species) even at pH 3.5, but no species-specific studies that have reported their presence in soil were tolerance could be observed under such conditions investigating acidic environments (Trân Van et al., 2000; (Table S1). Curtis et al., 2002; Salles et al., 2002; 2004; Belova et al., Based on this result, we hypothesized that members of 2006; Garau et al., 2009; Aizawa et al., 2010). For the Burkholderia genus would be favoured in low pH instance, Burkholderia unamae could only be isolated environments. We tested this hypothesis by analyzing the from the rhizosphere of plants growing in soils, with a pH relative abundance of soil Burkholderia in a trans- ranging from 4.5 to 7.1, but not from soils with a pH higher continental sample collection of 44 soils from a broad than 7.5 (Caballero-Mellado et al., 2004). Likewise, a array of ecosystem types that represent a wide range of survey of over 800 Australian soil samples revealed that soil and site characteristics (Table S2). The relative abun- B. pseudomallei was specifically associated with low pH dance of Burkholderia species greatly varied between soils, but not recovered from higher pH soils (Kaestli these different soils sampled across North and South et al., 2009). Burkholderia species have also been iso- America (Fig. 1A). Highest relative abundance was lated from acidic Sphagnum peat bogs (Belova et al., observed in moderately acidic soils (pH 5–pH 6), where 2006; Opelt et al., 2007a; 2007b), from root tissues of the up to 6.7% of the total bacterial population was repre- highly acidifying cluster rooted Lupinus albus (Weisskopf sented by Burkholderia species. It is worthwhile to notice et al., 2011) or from soils as acidic as pH 2.9 (Curtis et al., that within this pH range a large variability in Burkholderia 2002). To the best of our knowledge, only one study relative abundance was observed (standard devia- reported isolation of Burkholderia strains from an alkaline tion =±2.02), spanning from 0.04% to 6.25%, whereas in environment (Estrada-de los Santos et al., 2011). While more acidic soils (pH <4) relative abundances were the pH of the rhizosphere soil investigated in this study approximately 1% or higher. While high relative abun- © 2013 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology, 16, 1503–1512 Preference of Burkholderia sp. for acid soils 1505 3.5 to 6.8), C/N ratio, location and relative abundance of Burkholderia 16S rRNA genes were selected from the R = −0.76 trans-continental scale sampling set for phylogenetic analyses. Clone libraries targeting the 16S rRNA gene were constructed for each of the selected sites, and a total of 675 sequences (590 bp) were obtained, corresponding to 123 operational taxonomical units (OTUs) at a 98% identity threshold between Burkholderia 16S rRNA gene 0.05 0.10 0.15 0.20 sequences (Fig. 3). Diversity and richness of the soil Relative abundance (%) abundance Relative 0.00 Burkholderia communities were highly variable between 4.5 5.0 5.5 6.0 6.5 7.0 7.5 the sites, e.g.
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