Showing papers by "Thomas Bell published in 2011"

The bacterial biogeography of British soils.

Abstract: Despite recognition of the importance of soil bacteria to terrestrial ecosystem functioning there is little consensus on the factors regulating belowground biodiversity. Here we present a multi-scale spatial assessment of soil bacterial community profiles across Great Britain (> 1000 soil cores), and show the first landscape scale map of bacterial distributions across a nation. Bacterial diversity and community dissimilarities, assessed using terminal restriction fragment length polymorphism, were most strongly related to soil pH providing a large-scale confirmation of the role of pH in structuring bacterial taxa. However, while α diversity was positively related to pH, the converse was true for β diversity (between sample variance in α diversity). β diversity was found to be greatest in acidic soils, corresponding with greater environmental heterogeneity. Analyses of clone libraries revealed the pH effects were predominantly manifest at the level of broad bacterial taxonomic groups, with acidic soils being dominated by few taxa (notably the group 1 Acidobacteria and Alphaproteobacteria). We also noted significant correlations between bacterial communities and most other measured environmental variables (soil chemistry, aboveground features and climatic variables), together with significant spatial correlations at close distances. In particular, bacterial and plant communities were closely related signifying no strong evidence that soil bacteria are driven by different ecological processes to those governing higher organisms. We conclude that broad scale surveys are useful in identifying distinct soil biomes comprising reproducible communities of dominant taxa. Together these results provide a baseline ecological framework with which to pursue future research on both soil microbial function, and more explicit biome based assessments of the local ecological drivers of bacterial biodiversity.

Experimental niche evolution alters the strength of the diversity–productivity relationship

Abstract: The relationship between biodiversity and ecosystem functioning (BEF) has become a cornerstone of community and ecosystem ecology and an essential criterion for making decisions in conservation biology and policy planning. It has recently been proposed that evolutionary history should influence the BEF relationship because it determines species traits and, thus, species’ ability to exploit resources. Here we test this hypothesis by combining experimental evolution with a BEF experiment. We isolated 20 bacterial strains from a marine environment and evolved each to be generalists or specialists. We then tested the effect of evolutionary history on the strength of the BEF relationship with assemblages of 1 to 20 species constructed from the specialists, generalists and ancestors. Assemblages of generalists were more productive on average because of their superior ability to exploit the environmental heterogeneity. The slope of the BEF relationship was, however, stronger for the specialist assemblages because of enhanced niche complementarity. These results show how the BEF relationship depends critically on the legacy of past evolutionary events.

BUGS in the Analysis of Biodiversity Experiments: Species Richness and Composition Are of Similar Importance for Grassland Productivity

Abstract: The idea that species diversity can influence ecosystem functioning has been controversial and its importance relative to compositional effects hotly debated. Unfortunately, assessing the relative importance of different explanatory variables in complex linear models is not simple. In this paper we assess the relative importance of species richness and species composition in a multilevel model analysis of net aboveground biomass production in grassland biodiversity experiments by estimating variance components for all explanatory variables. We compare the variance components using a recently introduced graphical Bayesian ANOVA. We show that while the use of test statistics and the R2 gives contradictory assessments, the variance components analysis reveals that species richness and composition are of roughly similar importance for primary productivity in grassland biodiversity experiments.

Diet creates metabolic niches in the "immature gut" that shape microbial communities.

Abstract: Although diet composition has been implicated as a major factor in the etiology of various gastrointestinal diseases, conclusive evidence remains elusive. This is particularly true in diseases such as necrotizing enterocolitis where breast milk as opposed to commercial formula appears to confer a "protective effect" to the "immature gut." Yet the mechanism by which this occurs continues to remain speculative. In the present study we hypothesize that the basic chemical composition of diet fundamentally selects for specific intestinal microbiota which may help explain disparate disease outcome and therapeutic direction. Complimentary animal and human studies were conducted on young piglets (21 d.)(n = 8) (IACUC protocols 08070 and 08015) and premature infants (adjusted gestational age 34-36 weeks) (n = 11) (IRB Protocol 15895A). In each study, cecal or stool contents from two groups (Breast milk-fed (BF) vs. Formula-fed (FF)) were analyzed by gas chromatography/mass spectrometry (GC/MS) and comprehensive metabolic profiles generated and compared. Concurrently, bacterial community structure was assayed and respective representative microbiota of the groups determined by 16S rRNA gene amplicon pyrosequencing. Statistical modeling and analysis was done using SIMCA-P+ and R software. GC/MS metabolomics identified clear differences between BF and FF groups in the intestinal environment of piglets and humans. Sugars, amino-sugars, fatty acids, especially unsaturated fatty acids, and sterols were identified as being among the most important metabolites for distinguishing between BF and FF groups. Joint analysis of microbiota and metabolomics pinpointed specific sets of metabolites (p < 0.05) associated with the dominant bacterial taxa. The chemical composition of diet appears to have a significant role in defining the microbiota of the immature gut. Tandem analysis of intestinal microbial and metabolic profiles is potentially a powerful tool leading to better understanding of the role of diet in disease perhaps even leading to specific strategies to alter microbial behavior to improve clinical outcome.

Cheating, trade‐offs and the evolution of aggressiveness in a natural pathogen population

Abstract: The evolutionary and ecological mechanisms that maintain life-history variation in pathogens are fundamental to an understanding of disease emergence, epidemiology and infection outcomes (Ochman & Moran 2001; Barrett et al. 2008). Aggressiveness (i.e. within-host-fecundity), is among the most important of pathogen life-history traits, affecting the incidence and impact of pathogens in human, agricultural and natural systems. For the many pathogenic microbes that occur in genetically diverse populations (Read & Taylor 2001), classical theoretical investigations of virulence evolution predict that resource competition among competing strains favours strains with higher virulence, because more virulent strains are more aggressive and transmit at faster rates (May & Anderson 1983; Nowak & May 1994). However, results from recent empirical studies (Gower & Webster 2005; Staves & Knell 2010) suggest that evolution towards increased aggressiveness is not an inevitable outcome of within-host competition. Classical theory of pathogen evolution is therefore unlikely to be sufficient to describe evolution in mixed infections. Pathogenicity in many microbes depends on the secretion and acquisition of extracellular molecules that enhance performance via subversion of host immune responses and facilitation of access to host nutrients (Salmond 1994; Preston et al. 2005). These metabolically costly (Bartra et al. 2001; Griffin et al. 2004) pathogenicity factors modify the host environment for all co-occurring pathogen strains, and thus act as common goods (Frank 2010a) that may be exploited by non-secreting “cheater” strains (Chao et al. 2000; Brown et al. 2002; West & Buckling 2003). The secretion of common goods is thus a type of altruistic behaviour, the evolution of which has been shown by theory to require restrictive conditions. As a consequence, evolutionary theorists have sought to explain the maintenance of cooperative pathogen strains (Brown et al. 2002; Ross-Gillespie et al. 2007; West et al. 2007; Racey et al. 2010). In testing for cheating, previous studies have used strains that were experimentally evolved or artificially engineered to use extracellular molecules secreted by cooperator genotypes (Turner & Chao 1999; Griffin et al. 2004; Harrison et al. 2006). These experiments have confirmed a potential for cheating to occur under laboratory conditions, but whether such dynamics occur in nature is unclear. Meanwhile, theory to explain the maintenance of cooperator-cheater polymorphisms has focused on mechanisms that can be observed in vitro, notably on kin selection (Griffin et al. 2004). However, polymorphisms in nature may be maintained by mechanisms that are not apparent in vitro, eliminating the need for the moderate to high relatedness inherent in kin-selection models (Frank 2010b). Here we present the first evidence for a cooperator-cheater polymorphism in nature, and through a combination of data and models show that this polymorphism is likely maintained in part by a tradeoff between within-host and between-host reproduction. Studies of pathogen dynamics in vitro typically focus on competition in a single environment, i.e. within the host. However, pathogens may also compete outside of the host. Indeed, for the many ecologically and agriculturally important pathogens that are opportunistic, or maintain free living stages, survival and reproduction in the environment is likely to be essential. Such life-history strategies entail survival and propagation in non-host environments for long periods of time, enabling pathogens to persist when hosts are not present (Dwyer 1994; Bonhoeffer et al. 1996; Gandon 1998). Survival in the environment has been shown by models (Gandon 1998) to play a crucial role in pathogen competition, although the effect of reproduction outside the host has been rarely explored. One of our goals is to incorporate this life-history strategy into models of pathogen competition. Here, we investigate how within-host growth (i.e. aggressiveness) and reproduction in the environment together mediate bacterial competition in nature. We studied the pathogenic bacterium Pseudomonas syringae, which occurs at high frequency in populations of the plant Arabidopsis thaliana in the Midwestern U.S. (Kniskern et al. 2011). Pathogenic strains of P. syringae are natural parasites of A. thaliana (Jakob et al. 2002). While infections are typically sublethal, disease symptoms and pathogen densities within host plants are negatively related to host fecundity (Roux et al. 2010). Pseudomonas is a diverse and ubiquitous bacterial genus that includes species with a range of symbiotic and free-living life-histories. Pathogenicity in this group is facilitated by the Type Three Secretion System (TTSS) (Preston 2007), a needle-like apparatus that translocates effector proteins into host cells (Buttner & Bonas 2002). Collectively, effector proteins subvert host defences and facilitate the release of nutrients from host cells (Gohre & Robatzek 2008). Because P. syringae inhabits extra-cellular environments on the leaf surface and in the leaf mesophyll, benefits conferred by the TTSS and associated effectors have the potential to benefit neighbouring individuals even if nearby strains lack mechanisms facilitating pathogenicity. A further critical feature of P. syringae is its capacity for growth and survival as a free-living saprophyte in water and soil (Morris et al. 2008). Hypotheses for the maintenance of cooperation in this species can thus be framed around whether secretion of common goods within the host is negatively correlated with performance outside of the host. Importantly, the expression of the pathogenicity-promoting TTSS can be dependent on the environmental context in which growth occurs (Higuchi et al. 1959). For example TTSS expression in plant-pathogenic strains of P. syringae is activated in oligotrophic (low nutrient) environments (Huynh et al. 1989). Given that P. syringae is found in such environments outside of the host (Morris et al. 2008), and given that transmission among hosts may occur via environmental sources (e.g. from host contact with soil or rain) (Hollaway et al. 2007), the opportunity exists for energetic costs associated with the expression of the TTSS in host and non-host environments to modulate competition between strains and the maintenance of cooperation. The utility of the P. syringae-A. thaliana interaction for investigating the maintenance of pathogen variability is evidenced by the recent discovery of an apparently non-pathogenic P. syringae lineage carrying an aberrant TTSS (Mohr et al. 2008) (Supplementary Fig. 1). Strains of this lineage do not cause disease, have reduced capacity for growth in plants, are limited in their capacity to deliver effectors into host cells, and do not elicit the qualitative, innate immune response that is known as a hypersensitive response or ‘HR’ (Clarke et al. 2010; Kniskern et al. 2011). We therefore refer to strains carrying this aberrant TTSS as ‘HR-’, and strains carrying the canonical TTSS as ‘HR+’. Importantly, HR- strains have been found to co-occur with HR+ strains within wild A. thaliana populations (Kniskern et al. 2011). Given the established role that TTSS-secreted effectors play in pathogenesis and growth, the occurrence of a seemingly non-pathogenic clade of P. syringae begs the question of what ecological conditions might favour such an evolutionary transition. We thus asked two questions. First, do non-pathogenic HR- strains exhibit cheating behaviour? If so, does a tradeoff between reproduction in the host and reproduction in the environment help maintain a cooperator-cheater polymorphism in this system? Asking whether non-pathogenic strains cheat is equivalent to asking whether HR- strains compensate for reduced growth in planta via the exploitation of resources made publically available by HR+ strains (Brown 1999; Brown et al. 2002; Buckling & Brockhurst 2008). Asking whether reproduction in the environment helps to maintain the polymorphism is equivalent to asking whether HR- strains have a competitive advantage over HR+ strains when grown in the environment (Caraco & Wang 2008). To address these questions, we used a series of glasshouse and microcosm experiments in which we measured the growth of HR+ and HR- strains in planta (alone and in competition) and ex planta (in eutrophic and oligotrophic environments). In addition, we specifically investigated the role of TTSS polymorphisms in environmental fitness by performing a parallel set of experiments using genetically modified versions of HR+ and HR- strains. Finally, we developed a mathematical model to test the extent to which differences in competitive ability in within-host versus between-host environments promote the coexistence of HR+ and HR- strains of P. syringae.