Publications by authors named "Bruce C Thomson"

11 Publications

  • Page 1 of 1

Bacterial Physiological Adaptations to Contrasting Edaphic Conditions Identified Using Landscape Scale Metagenomics.

mBio 2017 07 5;8(4). Epub 2017 Jul 5.

Centre for Ecology and Hydrology, Wallingford, United Kingdom

Environmental factors relating to soil pH are important regulators of bacterial taxonomic biodiversity, yet it remains unclear if such drivers affect community functional potential. To address this, we applied whole-genome metagenomics to eight geographically distributed soils at opposing ends of a landscape soil pH gradient (where "low-pH" is ~pH 4.3 and "high-pH" is ~pH 8.3) and evaluated functional differences with respect to functionally annotated genes. First, differences in taxonomic and functional diversity between the two pH categories were assessed with respect to alpha diversity (mean sample richness) and gamma diversity (total richness pooled for each pH category). Low-pH soils, also exhibiting higher organic matter and moisture, consistently had lower taxonomic alpha and gamma diversity, but this was not apparent in assessments of functional alpha and gamma diversity. However, coherent changes in the relative abundances of annotated genes between low- and high-pH soils were identified; with strong multivariate clustering of samples according to pH independent of geography. Assessment of indicator genes revealed that the acidic organic-rich soils possessed a greater abundance of cation efflux pumps, C and N direct fixation systems, and fermentation pathways, indicating adaptations to both acidity and anaerobiosis. Conversely, high-pH soils possessed more direct transporter-mediated mechanisms for organic C and N substrate acquisition. These findings highlight the distinctive physiological adaptations required for bacteria to survive in soils of various nutrient availability and edaphic conditions and more generally indicate that bacterial functional versatility with respect to functional gene annotations may not be constrained by taxonomy. Over a set of soil samples spanning Britain, the widely reported reductions in bacterial taxonomic richness at low pH were found not to be accompanied by significant reductions in the richness of functional genes. However, consistent changes in the abundance of related functional genes were observed, characteristic of differential ecological and nutrient acquisition strategies between high-pH mineral soils and low-pH organic anaerobic soils. Our assessment at opposing ends of a soil gradient encapsulates the limits of functional diversity in temperate climates and identifies key pathways that may serve as indicators for soil element cycling and C storage processes in other soil systems. To this end, we make available a data set identifying functional indicators of the different soils; as well as raw sequences, which given the geographic scale of our sampling should be of value in future studies assessing novel genetic diversity of a wide range of soil functional attributes.
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http://dx.doi.org/10.1128/mBio.00799-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5573673PMC
July 2017

Soil networks become more connected and take up more carbon as nature restoration progresses.

Nat Commun 2017 02 8;8:14349. Epub 2017 Feb 8.

NIOO-KNAW, Microbial Ecology, Droevendaalsesteeg 10, Wageningen 6708 PB, The Netherlands.

Soil organisms have an important role in aboveground community dynamics and ecosystem functioning in terrestrial ecosystems. However, most studies have considered soil biota as a black box or focussed on specific groups, whereas little is known about entire soil networks. Here we show that during the course of nature restoration on abandoned arable land a compositional shift in soil biota, preceded by tightening of the belowground networks, corresponds with enhanced efficiency of carbon uptake. In mid- and long-term abandoned field soil, carbon uptake by fungi increases without an increase in fungal biomass or shift in bacterial-to-fungal ratio. The implication of our findings is that during nature restoration the efficiency of nutrient cycling and carbon uptake can increase by a shift in fungal composition and/or fungal activity. Therefore, we propose that relationships between soil food web structure and carbon cycling in soils need to be reconsidered.
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http://dx.doi.org/10.1038/ncomms14349DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5309817PMC
February 2017

Vegetation exerts a greater control on litter decomposition than climate warming in peatlands.

Ecology 2015 Jan;96(1):113-23

Historically, slow decomposition rates have resulted in the accumulation of large amounts of carbon in northern peatlands. Both climate warming and vegetation change can alter rates of decomposition, and hence affect rates of atmospheric CO2 exchange, with consequences for climate change feedbacks. Although warming and vegetation change are happening concurrently, little is known about their relative and interactive effects on decomposition processes. To test the effects of warming and vegetation change on decomposition rates, we placed litter of three dominant species (Calluna vulgaris, Eriophorum vaginatum, Hypnum jutlandicum) into a peatland field experiment that combined warming.with plant functional group removals, and measured mass loss over two years. To identify potential mechanisms behind effects, we also measured nutrient cycling and soil biota. We found that plant functional group removals exerted a stronger control over short-term litter decomposition than did approximately 1 degrees C warming, and that the plant removal effect depended on litter species identity. Specifically, rates of litter decomposition were faster when shrubs were removed from the plant community, and these effects were strongest for graminoid and bryophyte litter. Plant functional group removals also had strong effects on soil biota and nutrient cycling associated with decomposition, whereby shrub removal had cascading effects on soil fungal community composition, increased enchytraeid abundance, and increased rates of N mineralization. Our findings demonstrate that, in addition to litter quality, changes in vegetation composition play a significant role in regulating short-term litter decomposition and belowground communities in peatland, and that these impacts can be greater than moderate warming effects. Our findings, albeit from a relatively short-term study, highlight the need to consider both vegetation change and its impacts below ground alongside climatic effects when predicting future decomposition rates and carbon storage in peatlands.
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http://dx.doi.org/10.1890/14-0292.1DOI Listing
January 2015

Rhizosphere bacterial carbon turnover is higher in nucleic acids than membrane lipids: implications for understanding soil carbon cycling.

Front Microbiol 2015 9;6:268. Epub 2015 Apr 9.

Department of Biogeochemical Processes, Max Planck Institute for Biogeochemistry Jena, Germany.

Using a pulse chase (13)CO2 plant labeling experiment we compared the flow of plant carbon into macromolecular fractions of rhizosphere soil microorganisms. Time dependent (13)C dilution patterns in microbial cellular fractions were used to calculate their turnover time. The turnover times of microbial biomolecules were found to vary: microbial RNA (19 h) and DNA (30 h) turned over fastest followed by chloroform fumigation extraction-derived soluble cell lysis products (14 days), while phospholipid fatty acids (PLFAs) had the slowest turnover (42 days). PLFA/NLFA (13)C analyses suggest that both mutualistic arbuscular mycorrhizal and saprophytic fungi are dominant in initial plant carbon uptake. In contrast, high initial (13)C enrichment in RNA hints at bacterial importance in initial C uptake due to the dominance of bacterial derived RNA in total extracts of soil RNA. To explain this discrepancy, we observed low renewal rate of bacterial lipids, which may therefore bias lipid fatty acid based interpretations of the role of bacteria in soil microbial food webs. Based on our findings, we question current assumptions regarding plant-microbe carbon flux and suggest that the rhizosphere bacterial contribution to plant assimilate uptake could be higher. This highlights the need for more detailed quantitative investigations with nucleic acid biomarkers to further validate these findings.
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http://dx.doi.org/10.3389/fmicb.2015.00268DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4391234PMC
April 2015

Plant diversity increases soil microbial activity and soil carbon storage.

Nat Commun 2015 Apr 7;6:6707. Epub 2015 Apr 7.

Max Planck Institute for Biogeochemistry, POB 100164, 07701 Jena, Germany.

Plant diversity strongly influences ecosystem functions and services, such as soil carbon storage. However, the mechanisms underlying the positive plant diversity effects on soil carbon storage are poorly understood. We explored this relationship using long-term data from a grassland biodiversity experiment (The Jena Experiment) and radiocarbon ((14)C) modelling. Here we show that higher plant diversity increases rhizosphere carbon inputs into the microbial community resulting in both increased microbial activity and carbon storage. Increases in soil carbon were related to the enhanced accumulation of recently fixed carbon in high-diversity plots, while plant diversity had less pronounced effects on the decomposition rate of existing carbon. The present study shows that elevated carbon storage at high plant diversity is a direct function of the soil microbial community, indicating that the increase in carbon storage is mainly limited by the integration of new carbon into soil and less by the decomposition of existing soil carbon.
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http://dx.doi.org/10.1038/ncomms7707DOI Listing
April 2015

Plant soil interactions alter carbon cycling in an upland grassland soil.

Front Microbiol 2013 10;4:253. Epub 2013 Sep 10.

Centre for Ecology and Hydrology Wallingford, Oxfordshire, UK.

Soil carbon (C) storage is dependent upon the complex dynamics of fresh and native organic matter cycling, which are regulated by plant and soil-microbial activities. A fundamental challenge exists to link microbial biodiversity with plant-soil C cycling processes to elucidate the underlying mechanisms regulating soil carbon. To address this, we contrasted vegetated grassland soils with bare soils, which had been plant-free for 3 years, using stable isotope ((13)C) labeled substrate assays and molecular analyses of bacterial communities. Vegetated soils had higher C and N contents, biomass, and substrate-specific respiration rates. Conversely, following substrate addition unlabeled, native soil C cycling was accelerated in bare soil and retarded in vegetated soil; indicative of differential priming effects. Functional differences were reflected in bacterial biodiversity with Alphaproteobacteria and Acidobacteria dominating vegetated and bare soils, respectively. Significant isotopic enrichment of soil RNA was found after substrate addition and rates varied according to substrate type. However, assimilation was independent of plant presence which, in contrast to large differences in (13)CO2 respiration rates, indicated greater substrate C use efficiency in bare, Acidobacteria-dominated soils. Stable isotope probing (SIP) revealed most community members had utilized substrates with little evidence for competitive outgrowth of sub-populations. Our findings support theories on how plant-mediated soil resource availability affects the turnover of different pools of soil carbon, and we further identify a potential role of soil microbial biodiversity. Specifically we conclude that emerging theories on the life histories of dominant soil taxa can be invoked to explain changes in soil carbon cycling linked to resource availability, and that there is a strong case for considering microbial biodiversity in future studies investigating the turnover of different pools of soil carbon.
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http://dx.doi.org/10.3389/fmicb.2013.00253DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3767910PMC
September 2013

Mycobacterium avium subspecies paratuberculosis is widely distributed in British soils and waters: implications for animal and human health.

Environ Microbiol 2013 Oct 6;15(10):2761-74. Epub 2013 May 6.

Centre for Ecology and Hydrology, Lancaster Environment Centre, Lancaster, LA1 4AP, UK.

In the first comprehensive geographical survey of distribution in Great Britain, Mycobacterium avium ssp. paratuberculosis (MAP) was detected in 115 of 1092 (10.5%) soil cores, in the range of 5 × 10(2) to 3 × 10(6) MAP cell equivalents (CE) g(-1) wet weight soil with the majority of the positive PCR reactions (n = 75; 65%) occurring around the limit of detection (500-5000 CE g(-1) wet weight soil). The distribution of MAP significantly increased from North to South and was significantly correlated with increasing cattle numbers over the same longitudinal axis. Similarly MAP occurrence significantly increased towards easterly latitudes although none of the parameters measured were associated. Comparisons of land use indicated that MAP was widely distributed in both farming and non-farming areas. Soil core samples taken from the rivers Wyre and Douglas catchments (Lancashire, UK) and river Tywi (South Wales) were negative for MAP. However, river monitoring showed a consistent presence of MAPs throughout those catchments over a 6-month period. We concluded that MAP is widely distributed within and outside the confines of the farming environment; its geographical distribution is wider than originally anticipated and; monitoring rivers describes the MAP status of catchment better than individual soil samples.
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http://dx.doi.org/10.1111/1462-2920.12137DOI Listing
October 2013

Niche specialization of terrestrial archaeal ammonia oxidizers.

Proc Natl Acad Sci U S A 2011 Dec 8;108(52):21206-11. Epub 2011 Dec 8.

Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 3UU, United Kingdom.

Soil pH is a major determinant of microbial ecosystem processes and potentially a major driver of evolution, adaptation, and diversity of ammonia oxidizers, which control soil nitrification. Archaea are major components of soil microbial communities and contribute significantly to ammonia oxidation in some soils. To determine whether pH drives evolutionary adaptation and community structure of soil archaeal ammonia oxidizers, sequences of amoA, a key functional gene of ammonia oxidation, were examined in soils at global, regional, and local scales. Globally distributed database sequences clustered into 18 well-supported phylogenetic lineages that dominated specific soil pH ranges classified as acidic (pH <5), acido-neutral (5 ≤ pH <7), or alkalinophilic (pH ≥ 7). To determine whether patterns were reproduced at regional and local scales, amoA gene fragments were amplified from DNA extracted from 47 soils in the United Kingdom (pH 3.5-8.7), including a pH-gradient formed by seven soils at a single site (pH 4.5-7.5). High-throughput sequencing and analysis of amoA gene fragments identified an additional, previously undiscovered phylogenetic lineage and revealed similar pH-associated distribution patterns at global, regional, and local scales, which were most evident for the five most abundant clusters. Archaeal amoA abundance and diversity increased with soil pH, which was the only physicochemical characteristic measured that significantly influenced community structure. These results suggest evolution based on specific adaptations to soil pH and niche specialization, resulting in a global distribution of archaeal lineages that have important consequences for soil ecosystem function and nitrogen cycling.
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http://dx.doi.org/10.1073/pnas.1109000108DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3248517PMC
December 2011

The bacterial biogeography of British soils.

Environ Microbiol 2011 Jun 20;13(6):1642-54. Epub 2011 Apr 20.

Centre for Ecology & Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, Oxfordshire, OX10 8BB, UK.

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.
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http://dx.doi.org/10.1111/j.1462-2920.2011.02480.xDOI Listing
June 2011

Effects of sieving, drying and rewetting upon soil bacterial community structure and respiration rates.

J Microbiol Methods 2010 Oct 4;83(1):69-73. Epub 2010 Aug 4.

Centre for Ecology Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, OX10 8BB, United Kingdom.

Soil microcosm studies often require some form of soil homogenisation, such as sieving, to provide a representative sample. Frequently, soils are also homogenised following drying and are then rewetted, yet little research has been done to understand how these methods impact upon microbial communities. Here we compared the molecular diversity and functional responses of intact cores from a Scottish grassland soil with homogenised samples prepared by drying, sieving and rewetting or freshly sieving wet soils. Results showed that there was no significant difference in total soil CO(2)-C efflux between the freshly sieved and intact core treatments, however, respiration was significantly higher in the dried and rewetted microcosms. Molecular fingerprinting (T-RFLP) of bacterial communities at two different time-points showed that both homogenisation methods significantly altered bacterial community structure with the largest differences being observed after drying and rewetting. Assessments of responsive taxa in each treatment showed that intact cores were dominated by Acidobacterial peaks whereas an increased relative abundance of Alphaproteobacterial terminal restriction fragments were apparent in both homogenised treatments. However, the shift in community structure was not as large in the freshly sieved soil. Our findings suggest that if soil homogenisation must be performed, then fresh sieving of wet soil is preferable to drying and rewetting in approximating the bacterial diversity and functioning of intact cores.
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http://dx.doi.org/10.1016/j.mimet.2010.07.021DOI Listing
October 2010

Vegetation affects the relative abundances of dominant soil bacterial taxa and soil respiration rates in an upland grassland soil.

Microb Ecol 2010 Feb 25;59(2):335-43. Epub 2009 Aug 25.

Centre for Ecology & Hydrology, Oxford OX1 3SR, UK.

Plant-derived organic matter inputs are thought to be a key driver of soil bacterial community composition and associated soil processes. We sought to investigate the role of acid grassland vegetation on soil bacterial community structure by assessing bacterial diversity in combination with other soil variables in temporally and spatially distinct samples taken from a field-based plant removal experiment. Removal of aboveground vegetation resulted in reproducible differences in soil properties, soil respiration and bacterial diversity. Vegetated soils had significantly increased carbon and nitrogen concentrations and exhibited higher rates of respiration. Molecular analyses revealed that the soils were broadly dominated by Alphaproteobacterial and Acidobacterial lineages, with increased abundances of Alphaproteobacteria in vegetated soils and more Acidobacteria in bare soils. This field-based study contributes to a growing body of evidence documenting the effect of soil nutrient status on the relative abundances of dominant soil bacterial taxa, with Proteobacterial taxa dominating over Acidobacteria in soils exhibiting higher rates of C turnover. Furthermore, we highlight the role of aboveground vegetation in mediating this effect by demonstrating that plant removal can alter the relative abundances of dominant soil taxa with concomitant changes in soil CO(2)-C efflux.
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http://dx.doi.org/10.1007/s00248-009-9575-zDOI Listing
February 2010