Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

    Full text documents are added when available. The database is updated daily and currently holds about 240,000 items, of which 72,000 in open access.

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Soil bacterial community structure and functional responses across a long-term mineral phosphorus (Pi) fertilisation gradient differ in grazed and cut grasslands
Randall, Kate ; Brennan, Fiona ; Clipson, Nicholas ; Creamer, Rachel ; Griffiths, Bryan ; Storey, Sean ; Doyle, Evelyn - \ 2019
Applied Soil Ecology 138 (2019). - ISSN 0929-1393 - p. 134 - 143.
Agricultural management - Bacteria - Grassland - Phosphorus - Soil
Grasslands form a significant proportion of land used across the globe and future management is important. The objective of this study was to compare the long-term impact of inorganic phosphorus (Pi) fertilisation rates (P0, P15 and P30 ha−1 yr−1) under two grass management trials (grazed vs. cut and removed) on soil physicochemical properties, microbial biomass, phosphomonoesterase activity, bacterial community structure and abundance of a phosphorus (P) mineralising gene (phoD). Under grazing, microbial biomass and soil phosphorus concentrations (total and Pi) generally increased with Pi fertilisation rate, accompanied by significant differences in bacterial community structure between unfertilised (P0) and P30 soil. At the cut and removed site, although Pi was significantly greater in P30 soil, P concentrations (total and Pi) did not increase to the same extent as for grazing, with microbial biomass and bacterial community structures unresponsive to Pi fertilisation. Despite differences in soil P concentrations (total and Pi) and microbial biomass between sites, the abundance of bacterial phoD increased with increasing soil Pi across both sites, while phosphomonoesterase activity decreased. Amplicon sequencing revealed Acidobacteria were the dominant bacterial phylum across both grasslands, but significant differences in relative abundances of bacterial genera were detected at the grazed site only. The bacterial genera Gp6 and Gp16 increased significantly with Pi fertilisation under grazing. Conversely, Bradyrhizobium as well as unclassified genus-type groups belonging to Actinobacteria and Acidimicrobiales significantly decreased with Pi fertilisation, suggesting potential roles in P mobilisation when soil Pi concentrations are low. This study highlights the importance of long-term Pi fertilisation rates and aboveground vegetation removal in shaping soil bacterial community structure and microbial biomass, which in turn may impact soil fertility and plant productivity within agricultural soils.
Soil parameters, land use, and geographical distance drive soil bacterial communities along a European transect
Plassart, Pierre ; Prévost-Bouré, Nicolas Chemidlin ; Uroz, Stéphane ; Dequiedt, Samuel ; Stone, Dorothy ; Creamer, Rachel ; Griffiths, Robert I. ; Bailey, Mark J. ; Ranjard, Lionel ; Lemanceau, Philippe - \ 2019
Scientific Reports 9 (2019). - ISSN 2045-2322

To better understand the relationship between soil bacterial communities, soil physicochemical properties, land use and geographical distance, we considered for the first time ever a European transect running from Sweden down to Portugal and from France to Slovenia. We investigated 71 sites based on their range of variation in soil properties (pH, texture and organic matter), climatic conditions (Atlantic, alpine, boreal, continental, Mediterranean) and land uses (arable, forest and grassland). 16S rRNA gene amplicon pyrosequencing revealed that bacterial communities highly varied in diversity, richness, and structure according to environmental factors. At the European scale, taxa area relationship (TAR) was significant, supporting spatial structuration of bacterial communities. Spatial variations in community diversity and structure were mainly driven by soil physicochemical parameters. Within soil clusters (k-means approach) corresponding to similar edaphic and climatic properties, but to multiple land uses, land use was a major driver of the bacterial communities. Our analyses identified specific indicators of land use (arable, forest, grasslands) or soil conditions (pH, organic C, texture). These findings provide unprecedented information on soil bacterial communities at the European scale and on the drivers involved; possible applications for sustainable soil management are discussed.

Assignment of a dubious gene cluster to melanin biosynthesis in the tomato fungal pathogen Cladosporium fulvum
Griffiths, Scott A. ; Cox, Russell J. ; Overdijk, Elysa J.R. ; Mesarich, Carl H. ; Saccomanno, Benedetta ; Lazarus, Colin M. ; Wit, Pierre J.G.M. de; Collemare, Jérôme - \ 2018
PLoS ONE 13 (2018)12. - ISSN 1932-6203

Pigments and phytotoxins are crucial for the survival and spread of plant pathogenic fungi. The genome of the tomato biotrophic fungal pathogen Cladosporium fulvum contains a predicted gene cluster (CfPKS1, CfPRF1, CfRDT1 and CfTSF1) that is syntenic with the characterized elsinochrome toxin gene cluster in the citrus pathogen Elsinoë fawcettii. However, a previous phylogenetic analysis suggested that CfPks1 might instead be involved in pigment production. Here, we report the characterization of the CfPKS1 gene cluster to resolve this ambiguity. Activation of the regulator CfTSF1 specifically induced the expression of CfPKS1 and CfRDT1, but not of CfPRF1. These co-regulated genes that define the CfPKS1 gene cluster are orthologous to genes involved in 1,3-dihydroxynaphthalene (DHN) melanin biosynthesis in other fungi. Heterologous expression of CfPKS1 in Aspergillus oryzae yielded 1,3,6,8-tetrahydroxynaphthalene, a typical precursor of DHN melanin. Δcfpks1 deletion mutants showed similar altered pigmentation to wild type treated with DHN melanin inhibitors. These mutants remained virulent on tomato, showing this gene cluster is not involved in pathogenicity. Altogether, our results showed that the CfPKS1 gene cluster is involved in the production of DHN melanin and suggests that elsinochrome production in E. fawcettii likely involves another gene cluster.

Applying soil health indicators to encourage sustainable soil use : The transition from scientific study to practical application
Griffiths, Bryan S. ; Faber, Jack ; Bloem, Jaap - \ 2018
Sustainability 10 (2018)9. - ISSN 2071-1050
Earthworms - Ecosystem services - Monitoring - Soil food web - Water infiltration

The sustainable management of land for agricultural production has at its core a healthy soil, because this reduces the quantity of external inputs, reduces losses of nutrients to the environment, maximises the number of days when the soil can be worked, and has a pore structure that maximises both the retention of water in dry weather and drainage of water in wet weather. Soil health encompasses the physical, chemical, and biological features, but the use of biological indicators is the least well advanced. Sustainability also implies the balanced provision of ecosystem services, which can be more difficult to measure than single indicators. We describe how the key components of the soil food web contribute to a healthy soil and give an overview of the increasing number of scientific studies that have examined the use of biological indicators. A case study is made of the ecosystem service of water infiltration, which is quite an undertaking to measure directly, but which can be inferred from earthworm abundance and biodiversity which is relatively easy to measure. This highlights the difficulty of putting any monitoring scheme into practice and we finish by providing the considerations in starting a new soil health monitoring service in the UK and in maintaining biological monitoring in The Netherlands.

The need for standardisation : Exemplified by a description of the diversity, community structure and ecological indices of soil nematodes
Griffiths, B.S. ; Groot, G.A. de; Laros, I. ; Stone, D. ; Geisen, S. - \ 2018
Ecological Indicators 87 (2018). - ISSN 1470-160X - p. 43 - 46.
Biodiversity - DNA extraction - Metabarcoding - Microscopy - Molecular approaches - Nematodes - Standardisation
Molecular approaches are offering a supplement to, or even the possibility of replacing morphological identification of soil fauna, because of advantages for throughput, coverage and objectivity. We determined ecological indices of nematode community data from four sets of duplicate soil cores, based on morphological identification of nematodes after elutriation from 200 g soil and high throughput sequencing (HTS) targeting nematodes both after being elutriated from soils and DNA extracted directly from 10 g soil. HTS (at genus and species level) increased the taxonomic resolution compared to morphology (at family level). DNA extracted from elutriated nematodes identified more nematode taxa than when extracted from soil, due to an enrichment in nematode sequences. Each method also gave a different ecological footprint for the nematode community. Standardisation to previously determined indices based on morphological identification is needed in order to provide more meaningful information about soil quality and for ecological monitoring.
Detecting macroecological patterns in bacterial communities across independent studies of global soils
Ramirez, Kelly S. ; Knight, Christopher G. ; Hollander, Mattias de; Brearley, Francis Q. ; Constantinides, Bede ; Cotton, Anne ; Creer, Si ; Crowther, Thomas W. ; Davison, John ; Delgado-Baquerizo, Manuel ; Dorrepaal, Ellen ; Elliott, David R. ; Fox, Graeme ; Griffiths, Robert I. ; Hale, Chris ; Hartman, Kyle ; Houlden, Ashley ; Jones, David L. ; Krab, Eveline J. ; Maestre, Fernando T. ; McGuire, Krista L. ; Monteux, Sylvain ; Orr, Caroline H. ; Putten, Wim H. van der; Roberts, Ian S. ; Robinson, David A. ; Rocca, Jennifer D. ; Rowntree, Jennifer ; Schlaeppi, Klaus ; Shepherd, Matthew ; Singh, Brajesh K. ; Straathof, Angela L. ; Bhatnagar, Jennifer M. ; Thion, Cécile ; Heijden, Marcel G.A. van der; Vries, Franciska T. de - \ 2018
Nature Microbiology 3 (2018). - ISSN 2058-5276 - p. 189 - 196.
The emergence of high-throughput DNA sequencing methods provides unprecedented opportunities to further unravel bacterial biodiversity and its worldwide role from human health to ecosystem functioning. However, despite the abundance of sequencing studies, combining data from multiple individual studies to address macroecological questions of bacterial diversity remains methodically challenging and plagued with biases. Here, using a machine-learning approach that accounts for differences among studies and complex interactions among taxa, we merge 30 independent bacterial data sets comprising 1,998 soil samples from 21 countries. Whereas previous meta-analysis efforts have focused on bacterial diversity measures or abundances of major taxa, we show that disparate amplicon sequence data can be combined at the taxonomy-based level to assess bacterial community structure. We find that rarer taxa are more important for structuring soil communities than abundant taxa, and that these rarer taxa are better predictors of community structure than environmental factors, which are often confounded across studies. We conclude that combining data from independent studies can be used to explore bacterial community dynamics, identify potential ‘indicator’ taxa with an important role in structuring communities, and propose hypotheses on the factors that shape bacterial biogeography that have been overlooked in the past.
Specific Hypersensitive Response–Associated Recognition of New Apoplastic Effectors from Cladosporium fulvum in Wild Tomato
Mesarich, Carl H. ; Ӧkmen, Bilal ; Rovenich, Hanna ; Griffiths, Scott A. ; Wang, Changchun ; Karimi Jashni, Mansoor ; Mihajlovski, Aleksandar ; Collemare, Jérôme ; Hunziker, Lukas ; Deng, Cecilia H. ; Burgt, Ate Van Der; Beenen, Henriek G. ; Templeton, Matthew D. ; Bradshaw, Rosie E. ; Wit, Pierre J.G.M. De - \ 2018
Molecular Plant-Microbe Interactions 31 (2018)1. - ISSN 0894-0282 - p. 145 - 162.
Tomato leaf mold disease is caused by the biotrophic fungus Cladosporium fulvum. During infection, C. fulvum produces extracellular small secreted protein (SSP) effectors that function to promote colonization of the leaf apoplast. Resistance to the disease is governed by Cf immune receptor genes that encode receptor-like proteins (RLPs). These RLPs recognize specific SSP effectors to initiate a hypersensitive response (HR) that renders the pathogen avirulent. C. fulvum strains capable of overcoming one or more of all cloned Cf genes have now emerged. To combat these strains, new Cf genes are required. An effectoromics approach was employed to identify wild tomato accessions carrying new Cf genes. Proteomics and transcriptome sequencing were first used to identify 70 apoplastic in planta–induced C. fulvum SSPs. Based on sequence homology, 61 of these SSPs were novel or lacked known functional domains. Seven, however, had predicted structural homology to antimicrobial proteins, suggesting a possible role in mediating antagonistic microbe-microbe interactions in planta. Wild tomato accessions were then screened for HR-associated recognition of 41 SSPs, using the Potato virus X–based transient expression system. Nine SSPs were recognized by one or more accessions, suggesting that these plants carry new Cf genes available for incorporation into cultivated tomato.
Down-regulation of cladofulvin biosynthesis is required for biotrophic growth of Cladosporium fulvum on tomato : A secondary metabolite prevents fungal biotrophy
Griffiths, Scott ; Mesarich, Carl H. ; Overdijk, Elysa J.R. ; Saccomanno, Benedetta ; Wit, Pierre J.G.M. De; Collemare, Jérôme - \ 2018
Molecular Plant Pathology 19 (2018)2. - ISSN 1464-6722 - p. 369 - 380.
Fungal biotrophy is associated with a reduced capacity to produce potentially toxic secondary metabolites (SMs). Yet, the genome of the biotrophic plant pathogen Cladosporium fulvum contains many SM biosynthetic gene clusters, with several related to toxin production. These gene clusters are, however, poorly expressed during colonisation of tomato. The sole detectable SM produced by C. fulvum during in vitro growth is the anthraquinone cladofulvin. Although this pigment is not detected in infected leaves, cladofulvin biosynthetic genes are expressed throughout the pre-penetration phase and during conidiation at the end of the infection cycle, but they are repressed during the biotrophic phase of tomato colonization. It was suggested that tight regulation of SM gene clusters is required for C. fulvum to behave as a biotrophic pathogen, while retaining potential fitness determinants for growth and survival outside its host. To address this hypothesis, we analysed the disease symptoms caused by mutant C. fulvum strains that do not produce or over-produce cladofulvin during the biotrophic growth phase. Non-producers infected tomato similar to wild type, suggesting that cladofulvin is not a virulence factor. In contrast, the cladofulvin over-producers caused strong necrosis and desiccation of tomato leaves, which in turn, arrested conidiation. Consistent with the role of pigments in survival against abiotic stresses, cladofulvin protects conidia against UV light and low temperature stress. Overall this study demonstrates that repression of cladofulvin production is required for C. fulvum to sustain its biotrophic lifestyle in tomato, while its production is important for survival outside its host.
Isolation by oceanic distance and spatial genetic structure in an overharvested international fishery
Truelove, Nathan K. ; Box, Stephen J. ; Aiken, Karl A. ; Blythe-Mallett, Azra ; Boman, Erik M. ; Booker, Catherine J. ; Byfield, Tamsen T. ; Cox, Courtney E. ; Davis, Martha H. ; Delgado, Gabriel A. ; Glazer, Bob A. ; Griffiths, Sarah M. ; Kitson-Walters, Kimani ; Kough, Andy S. ; Pérez Enríquez, Ricardo ; Preziosi, Richard F. ; Roy, Marcia E. ; Segura-García, Iris ; Webber, Mona K. ; Stoner, Allan W. - \ 2017
Diversity and Distributions 23 (2017)11. - ISSN 1366-9516 - p. 1292 - 1300.
Connectivity - Conservation - Dispersal - Fisheries - Genetics - Spatial

Aim: A detailed understanding of spatial genetic structure (SGS) and the factors driving contemporary patterns of gene flow and genetic diversity are fundamental for developing conservation and management plans for marine fisheries. We performed a detailed study of SGS and genetic diversity throughout the overharvested queen conch (Lobatus gigas) fishery. Caribbean countries were presented as major populations to examine transboundary patterns of population differentiation. Location: Nineteen locations in the greater Caribbean from Anguilla, the Bahamas, Belize, Caribbean Netherlands, Honduras, Jamaica, Mexico, Turks and Caicos, and the USA. Methods: We genotyped 643 individuals with nine microsatellites. Population genetic and multivariate analyses characterized SGS. We tested the alternate hypotheses: (1) SGS is randomly distributed in space or (2) pairwise genetic structure among sites is correlated with oceanic distance (IBOD). Results: Our study found that L. gigas does not form a single panmictic population in the greater Caribbean. Significant levels of genetic differentiation were identified between Caribbean countries (FCT = 0.011; p = .0001), within Caribbean countries (FSC = 0.003; p = .001), and among sites irrespective of geographic location (FST = 0.013; p = .0001). Gene flow across the greater Caribbean was constrained by oceanic distance (p = .0009; Mantel r = .40), which acted to isolate local populations. Main conclusions: Gene flow over the spatial scale of the entire Caribbean basin is constrained by oceanic distance, which may impede the natural recovery of overfished L. gigas populations. Our results suggest a careful blend of local and international management will be required to ensure long-term sustainability for the species.

Priorities for research in soil ecology
Eisenhauer, Nico ; Antunes, Pedro M. ; Bennett, Alison E. ; Birkhofer, Klaus ; Bissett, Andrew ; Bowker, Matthew A. ; Caruso, Tancredi ; Chen, Baodong ; Coleman, David C. ; Boer, Wietse de; Ruiter, Peter de; DeLuca, Thomas H. ; Frati, Francesco ; Griffiths, Bryan S. ; Hart, Miranda M. ; Hättenschwiler, Stephan ; Haimi, Jari ; Heethoff, Michael ; Kaneko, Nobuhiro ; Kelly, Laura C. ; Leinaas, Hans Petter ; Lindo, Zoë ; Macdonald, Catriona ; Rillig, Matthias C. ; Ruess, Liliane ; Scheu, Stefan ; Schmidt, Olaf ; Seastedt, Timothy R. ; Straalen, Nico M. van; Tiunov, Alexei V. ; Zimmer, Martin ; Powell, Jeff R. - \ 2017
Pedobiologia 63 (2017). - ISSN 0031-4056 - p. 1 - 7.
Aboveground-belowground interactions - Biodiversity–ecosystem functioning - Biogeography - Chemical ecology - Climate change - Ecosystem services - Global change - Microbial ecology - Novel environments - Plant-microbe interactions - Soil biodiversity - Soil food web - Soil management - Soil processes
The ecological interactions that occur in and with soil are of consequence in many ecosystems on the planet. These interactions provide numerous essential ecosystem services, and the sustainable management of soils has attracted increasing scientific and public attention. Although soil ecology emerged as an independent field of research many decades ago, and we have gained important insights into the functioning of soils, there still are fundamental aspects that need to be better understood to ensure that the ecosystem services that soils provide are not lost and that soils can be used in a sustainable way. In this perspectives paper, we highlight some of the major knowledge gaps that should be prioritized in soil ecological research. These research priorities were compiled based on an online survey of 32 editors of Pedobiologia – Journal of Soil Ecology. These editors work at universities and research centers in Europe, North America, Asia, and Australia. The questions were categorized into four themes: (1) soil biodiversity and biogeography, (2) interactions and the functioning of ecosystems, (3) global change and soil management, and (4) new directions. The respondents identified priorities that may be achievable in the near future, as well as several that are currently achievable but remain open. While some of the identified barriers to progress were technological in nature, many respondents cited a need for substantial leadership and goodwill among members of the soil ecology research community, including the need for multi-institutional partnerships, and had substantial concerns regarding the loss of taxonomic expertise.
Optimal nutrition and the ever-changing dietary landscape : a conference report
Shao, A. ; Drewnowski, A. ; Willcox, D.C. ; Krämer, L. ; Lausted, C. ; Eggersdorfer, M. ; Mathers, J. ; Bell, J.D. ; Randolph, R.K. ; Witkamp, R. ; Griffiths, J.C. - \ 2017
European Journal of Nutrition 56 (2017)suppl.1. - ISSN 1436-6207 - 21 p.
Aging - Big data - Bioactives - Biomarkers - Dietary patterns - Dietary supplements - Longevity - Micronutrients - Obesity - Overfed - Phytonutrients - Sarcopenic obesity - Systems approaches - Undernourished - Wellness

The field of nutrition has evolved rapidly over the past century. Nutrition scientists and policy makers in the developed world have shifted the focus of their efforts from dealing with diseases of overt nutrient deficiency to a new paradigm aimed at coping with conditions of excess—calories, sedentary lifestyles and stress. Advances in nutrition science, technology and manufacturing have largely eradicated nutrient deficiency diseases, while simultaneously facing the growing challenges of obesity, non-communicable diseases and aging. Nutrition research has gone through a necessary evolution, starting with a reductionist approach, driven by an ambition to understand the mechanisms responsible for the effects of individual nutrients at the cellular and molecular levels. This approach has appropriately expanded in recent years to become more holistic with the aim of understanding the role of nutrition in the broader context of dietary patterns. Ultimately, this approach will culminate in a full understanding of the dietary landscape—a web of interactions between nutritional, dietary, social, behavioral and environmental factors—and how it impacts health maintenance and promotion.

Soil protistology rebooted: 30 fundamental questions to start with
Geisen, Stefan ; Mitchell, Edward A.D. ; Wilkinson, David M. ; Adl, Sina ; Bonkowski, Michael ; Brown, Matthew W. ; Fiore-Donno, Anna Maria ; Heger, Thierry J. ; Jassey, Vincent E.J. ; Krashevska, Valentyna ; Lahr, Daniel J.G. ; Marcisz, Katarzyna ; Mulot, Matthieu ; Payne, Richard ; Singer, David ; Anderson, O.R. ; Charman, Dan J. ; Ekelund, Flemming ; Griffiths, Bryan S. ; Rønn, Regin ; Smirnov, Alexey ; Bass, David ; Belbahri, Lassaâd ; Berney, Cédric ; Blandenier, Quentin ; Chatzinotas, Antonis ; Clarholm, Marianne ; Dunthorn, Micah ; Feest, Alan ; Fernández, Leonardo D. ; Foissner, Wilhelm ; Fournier, Bertrand ; Gentekaki, Eleni ; Hájek, Michal ; Helder, Hans ; Jousset, Alexandre ; Koller, Robert ; Kumar, Santosh ; Terza, Antonietta La; Lamentowicz, Mariusz ; Mazei, Yuri ; Santos, Susana S. ; Seppey, Christophe V.W. ; Spiegel, Frederick W. ; Walochnik, Julia ; Winding, Anne ; Lara, Enrique - \ 2017
Soil Biology and Biochemistry 111 (2017). - ISSN 0038-0717 - p. 94 - 103.
Protists are the most diverse eukaryotes. These microbes are keystone organisms of soil ecosystems and
regulate essential processes of soil fertility such as nutrient cycling and plant growth. Despite this,
protists have received little scientific attention, especially compared to bacteria, fungi and nematodes in
soil studies. Recent methodological advances, particularly in molecular biology techniques, have made
the study of soil protists more accessible, and have created a resurgence of interest in soil protistology.
This ongoing revolution now enables comprehensive investigations of the structure and functioning of
soil protist communities, paving the way to a new era in soil biology. Instead of providing an exhaustive
review, we provide a synthesis of research gaps that should be prioritized in future studies of soil
protistology to guide this rapidly developing research area. Based on a synthesis of expert opinion we
propose 30 key questions covering a broad range of topics including evolution, phylogenetics, functional
ecology, macroecology, paleoecology, and methodologies. These questions highlight a diversity of topics
that will establish soil protistology as a hub discipline connecting different fundamental and applied
fields such as ecology, biogeography, evolution, plant-microbe interactions, agronomy, and conservation
biology. We are convinced that soil protistology has the potential to be one of the most exciting frontiers
in biology.
Soil networks become more connected and take up more carbon as nature restoration progresses
Morriën, W.E. ; Hannula, S.E. ; Snoek, L.B. ; Helmsing, N.R. ; Zweers, Hans ; Hollander, M. de; Soto, Raquel Luján ; Bouffaud, Marie Lara ; Buée, M. ; Dimmers, W.J. ; Duyts, Henk ; Geisen, Stefan ; Girlanda, Mariangela ; Griffiths, R.I. ; Jorgensen, H.B. ; Jensen, J. ; Plassart, P. ; Redecker, Dirk ; Schmelz, R.M. ; Schmidt, Olaf ; Thomson, Bruce C. ; Tisserant, Emilie ; Uroz, Stephane ; Winding, Anne ; Bailey, M.J. ; Bonkowski, M. ; Faber, J.H. ; Martin, F. ; Lemanceau, Philippe ; Boer, W. de; Veen, J.A. van; Putten, W.H. van der - \ 2017
Nature Communications 8 (2017). - ISSN 2041-1723 - 10 p.
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.
Selecting cost effective and policy-relevant biological indicators for European monitoring of soil biodiversity and ecosystem function
Griffiths, B.S. ; Römbke, J. ; Schmelz, R.M. ; Scheffczyk, A. ; Faber, J.H. ; Bloem, J. ; Peres, G. ; Cluzeau, D. ; Chabbi, A. ; Suhadolc, M. ; Sousa, J.P. ; Silva, P.M. da; Carvalho, F. ; Mendes, S. ; Morais, P. ; Francisco, R. ; Pereira, C. ; Bonkowski, M. ; Geisen, Stefan ; Bardgetti, R.D. ; Vries, F.T. De; Bolger, T. ; Dirilgen, T. ; Schmidt, O. ; Winding, Anne ; Hendriksen, Nicolien ; Johansen, A. ; Philippot, L. ; Plassart, P. ; Bru, D. ; Thomson, B.M. ; Griffiths, R.I. ; Bailey, Megan ; Keith, A. ; Rutgers, M. ; Mulder, Christian ; Hannula, S.E. ; Creamer, Rachel ; Stone, D. - \ 2016
Ecological Indicators 69 (2016). - ISSN 1470-160X - p. 213 - 223.
Soils provide many ecosystem services that are ultimately dependent on the local diversity and belowground abundance of organisms. Soil biodiversity is affected negatively by many threats and there is a perceived policy requirement for the effective biological monitoring of soils at the European level. The aim of this study was to evaluate and recommend policy relevant, cost-effective soil biological indicators for biodiversity and ecosystem function across Europe. A total of 18 potential indicators were selected using a logical-sieve based approach. This paper considers the use of indicators from the ‘top down’ (i.e. concerned with the process of indicator selection), rather than from the ‘bottom up’ detail of how individual indicators perform at specific sites and with specific treatments. The indicators assessed a range of microbial, faunal and functional attributes, newer nucleic acids based techniques, morphological approaches and process based measurements. They were tested at 6 European experimental sites already in operation and chosen according to land-use, climatic zone and differences in land management intensity. These were 4 arable sites, one each in Atlantic, Continental, Mediterranean and Pannonian climate zones, and 2 grassland sites, one each in Atlantic and Continental zones. At each site we sampled three replicated plots of contrasting management intensity and, while the treatments varied from site to site, their disturbance effects were quantified in terms of land use intensity. The field sampling and laboratory analysis were standardised through a combination of ISO protocols, or standard operating procedures if the former were not available. Sites were sampled twice, in autumn 2012 and spring or autumn 2013, with relative costs of the different indicators being determined each time. A breakdown of the cost effectiveness of the indicators showed the expected trade-off between effort required in the field and effort required in the laboratory. All the indicators were able to differentiate between the sites but, as no single indicator was sensitive to all the differences in land use intensity, we suggest that an indicator programme should be based upon a suite of different indicators. For monitoring under the European climatic zones and land uses of this study, indicators for ecosystem functions related to the services of water regulation, C-sequestration and nutrient provision would include a minimum suite of: earthworms; functional genes; and bait lamina. For effective monitoring of biodiversity all taxonomic groups would need to be addressed.
Novel effectors identified in the apoplast of Cladosporium fulvum-infected tomato
Mesarich, C. ; Ökmen, B. ; Rövenich, H.J. ; Karimi Jashni, M. ; Wang, C. ; Griffiths, S.A. ; Collemare, J.A.R. ; Deng, C. ; Wit, P.J.G.M. de - \ 2016
Tomato leaf mold disease is caused by the biotrophic fungal pathogen Cladosporium fulvum. To colonize the leaf apoplast, C. fulvum secretes a collection of effector proteins that modulate host immune responses, as well as other proteins (e.g., carbohydrate-active enzymes or CAZys) that facilitate nutrient acquisition. In the presence of cognate Cf immune receptors, however, many of these proteins trigger immune responses that render the pathogen avirulent. Characterization of the C. fulvum apoplastic secretome is required to further understand the abovementioned processes, and to identify novel sources of resistance against this pathogen. We have used liquid chromatography–tandem mass spectrometry (LC–MS/MS) to identify 141 secreted and surface-associated fungal proteins present in apoplastic fluid harvested from compatible C. fulvum–tomato interactions. In addition to the known effectors identified in previous studies, this collection contains >70 new C. fulvum candidate effector (CfCE) proteins. Using a Potato virus X (PVX)-based expression system, we show that nine of these CfCEs, including Ecp11-1, which has homology to AvrLm3 and AvrLmJ1 of Leptosphaeria maculans, trigger cell death in particular wild accessions of tomato. Thus, our study has likely uncovered novel avirulence effectors of C. fulvum, as well as Cf immune receptors in wild tomato with new specificities against this pathogen. An overview of the C. fulvum apoplastic secretome will be presented.
Lineage tracking for probing heritable phenotypes at single-cell resolution
Cottinet, Denis ; Condamine, Florence ; Bremond, Nicolas ; Griffiths, Andrew D. ; Rainey, Paul B. ; Visser, Arjan de; Baudry, Jean ; Bibette, Jérôme - \ 2016
PLoS ONE 11 (2016)4. - ISSN 1932-6203

Determining the phenotype and genotype of single cells is central to understand microbial evolution. DNA sequencing technologies allow the detection of mutants at high resolution, but similar approaches for phenotypic analyses are still lacking. We show that a drop-based millifluidic system enables the detection of heritable phenotypic changes in evolving bacterial populations. At time intervals, cells were sampled and individually compartmentalized in 100 nL drops. Growth through 15 generations was monitored using a fluorescent protein reporter. Amplification of heritable changes-via growth-over multiple generations yields phenotypically distinct clusters reflecting variation relevant for evolution. To demonstrate the utility of this approach, we follow the evolution of Escherichia coli populations during 30 days of starvation. Phenotypic diversity was observed to rapidly increase upon starvation with the emergence of heritable phenotypes. Mutations corresponding to each phenotypic class were identified by DNA sequencing. This scalable lineage-tracking technology opens the door to large-scale phenotyping methods with special utility for microbiology and microbial population biology.

Elucidation of cladofulvin biosynthesis reveals a cytochrome P450 monooxygenase required for anthraquinone dimerization
Griffiths, Scott ; Mesarich, Carl H. ; Saccomanno, Benedetta ; Vaisberg, Abraham ; Wit, Pierre J.G.M. de; Cox, Russell ; Collemare, Jérôme - \ 2016
Proceedings of the National Academy of Sciences of the United States of America 113 (2016)25. - ISSN 0027-8424 - p. 6851 - 6856.
Cytoxicity - Emodin - Gene cluster - Nataloe-emodin - Secondary metabolism

Anthraquinones are a large family of secondary metabolites (SMs) that are extensively studied for their diverse biological activities. These activities are determined by functional group decorations and the formation of dimers from anthraquinone monomers. Despite their numerous medicinal qualities, very few anthraquinone biosynthetic pathways have been elucidated so far, including the enzymatic dimerization steps. In this study, we report the elucidation of the biosynthesis of cladofulvin, an asymmetrical homodimer of nataloe-emodin produced by the fungus Cladosporium fulvum. A gene cluster of 10 genes controls cladofulvin biosynthesis, which begins with the production of atrochrysone carboxylic acid by the polyketide synthase ClaG and the β-lactamase ClaF. This compound is decarboxylated by ClaH to yield emodin, which is then converted to chrysophanol hydroquinone by the reductase ClaC and the dehydratase ClaB. We show that the predicted cytochrome P450 ClaM catalyzes the dimerization of nataloe-emodin to cladofulvin. Remarkably, such dimerization dramatically increases nataloe-emodin cytotoxicity against mammalian cell lines. These findings shed light on the enzymatic mechanisms involved in anthraquinone dimerization. Future characterization of the ClaM enzyme should facilitate engineering the biosynthesis of novel, potent, dimeric anthraquinones and structurally related compound families.

Climate seasonality limits leaf carbon assimilation and wood productivity in tropical forests
Wagner, Fabien H. ; Hérault, Bruno ; Bonal, Damien ; Stahl, Clément ; Anderson, Liana O. ; Baker, Timothy R. ; Becker, Gabriel Sebastian ; Beeckman, Hans ; Boanerges Souza, Danilo ; Botosso, Paulo Cesar ; Bowman, David M.J.S. ; Bräuning, Achim ; Brede, Benjamin ; Brown, Foster Irving ; Camarero, Jesus Julio ; Camargo, Plínio Barbosa ; Cardoso, Fernanda C.G. ; Carvalho, Fabrício Alvim ; Castro, Wendeson ; Chagas, Rubens Koloski ; Chave, Jérome ; Chidumayo, Emmanuel N. ; Clark, Deborah A. ; Costa, Flavia Regina Capellotto ; Couralet, Camille ; Silva Mauricio, Paulo Henrique Da; Dalitz, Helmut ; Castro, Vinicius Resende De; Freitas Milani, Jaçanan Eloisa De; Oliveira, Edilson Consuelo De; Souza Arruda, Luciano De; Devineau, Jean-Louis ; Drew, David M. ; Dünisch, Oliver ; Durigan, Giselda ; Elifuraha, Elisha ; Fedele, Marcio ; Ferreira Fedele, Ligia ; Figueiredo Filho, Afonso ; Finger, César Augusto Guimarães ; Franco, Augusto César ; Freitas Júnior, João Lima ; Galvão, Franklin ; Gebrekirstos, Aster ; Gliniars, Robert ; Lima De Alencastro Graça, Paulo Maurício ; Griffiths, Anthony D. ; Grogan, James ; Guan, Kaiyu ; Homeier, Jürgen ; Kanieski, Maria Raquel ; Kho, Lip Khoon ; Koenig, Jennifer ; Kohler, Sintia Valerio ; Krepkowski, Julia ; Lemos-filho, José Pires ; Lieberman, Diana ; Lieberman, Milton Eugene ; Lisi, Claudio Sergio ; Longhi Santos, Tomaz ; López Ayala, José Luis ; Maeda, Eduardo Eijji ; Malhi, Yadvinder ; Maria, Vivian R.B. ; Marques, Marcia C.M. ; Marques, Renato ; Maza Chamba, Hector ; Mbwambo, Lawrence ; Melgaço, Karina Liana Lisboa ; Mendivelso, Hooz Angela ; Murphy, Brett P. ; O'Brien, Joseph J. ; Oberbauer, Steven F. ; Okada, Naoki ; Pélissier, Raphaël ; Prior, Lynda D. ; Roig, Fidel Alejandro ; Ross, Michael ; Rossatto, Davi Rodrigo ; Rossi, Vivien ; Rowland, Lucy ; Rutishauser, Ervan ; Santana, Hellen ; Schulze, Mark ; Selhorst, Diogo ; Silva, Williamar Rodrigues ; Silveira, Marcos ; Spannl, Susanne ; Swaine, Michael D. ; Toledo, José Julio ; Toledo, Marcos Miranda ; Toledo, Marisol ; Toma, Takeshi ; Tomazello Filho, Mario ; Valdez Hernández, Juan Ignacio ; Verbesselt, Jan ; Vieira, Simone Aparecida ; Vincent, Grégoire ; Volkmer De Castilho, Carolina ; Volland, Franziska ; Worbes, Martin ; Zanon, Magda Lea Bolzan ; Aragão, Luiz E.O.C. - \ 2016
Biogeosciences 13 (2016)8. - ISSN 1726-4170 - p. 2537 - 2562.
The seasonal climate drivers of the carbon cycle in tropical forests remain poorly known, although these forests account for more carbon assimilation and storage than any other terrestrial ecosystem. Based on a unique combination of seasonal pan-tropical data sets from 89 experimental sites (68 include aboveground wood productivity measurements and 35 litter productivity measurements), their associated canopy photosynthetic capacity (enhanced vegetation index, EVI) and climate, we ask how carbon assimilation and aboveground allocation are related to climate seasonality in tropical forests and how they interact in the seasonal carbon cycle. We found that canopy photosynthetic capacity seasonality responds positively to precipitation when rainfall is  < 2000 mm yr−1 (water-limited forests) and to radiation otherwise (light-limited forests). On the other hand, independent of climate limitations, wood productivity and litterfall are driven by seasonal variation in precipitation and evapotranspiration, respectively. Consequently, light-limited forests present an asynchronism between canopy photosynthetic capacity and wood productivity. First-order control by precipitation likely indicates a decrease in tropical forest productivity in a drier climate in water-limited forest, and in current light-limited forest with future rainfall  < 2000 mm yr−1.
The EU societal awareness of landscape indicator : A review of its meaning, utility and performance across different scales
Jones, P.J. ; Andersen, E. ; Capitani, C. ; Carvalho Ribeiro, S. ; Griffiths, G.H. ; Loupa-Ramos, I. ; Madeira, L. ; Mortimer, S.R. ; Paracchini, M.L. ; Pinto Correia, T. ; Schmidt, A.M. ; Simoncini, R. ; Wascher, D.M. - \ 2016
Land Use Policy 53 (2016). - ISSN 0264-8377 - p. 112 - 122.
Geospatial indicators - Rural agrarian landscapes - Social and cultural values

There is increasing recognition that agricultural landscapes meet multiple societal needs and demands beyond provision of economic and environmental goods and services. Accordingly, there have been significant calls for the inclusion of societal, amenity and cultural values in agri-environmental landscape indicators to assist policy makers in monitoring the wider impacts of land-based policies. However, capturing the amenity and cultural values that rural agrarian areas provide, by use of such indicators, presents significant challenges. The EU social awareness of landscape indicator represents a new class of generalized social indicator using a top-down methodology to capture the social dimensions of landscape without reference to the specific structural and cultural characteristics of individual landscapes. This paper reviews this indicator in the context of existing agri-environmental indicators and their differing design concepts. Using a stakeholder consultation approach in five case study regions, the potential and limitations of the indicator are evaluated, with a particular focus on its perceived meaning, utility and performance in the context of different user groups and at different geographical scales. This analysis supplements previous EU-wide assessments, through regional scale assessment of the limitations and potentialities of the indicator and the need for further data collection. The evaluation finds that the perceived meaning of the indicator does not vary with scale, but in common with all mapped indicators, the usefulness of the indicator, to different user groups, does change with scale of presentation. This indicator is viewed as most useful when presented at the scale of governance at which end users operate. The relevance of the different sub-components of the indicator are also found to vary across regions.

Mite community composition across a European transect and its relationships to variation in other components of soil biodiversity
Dirilgen, T. ; Arroyo, J. ; Dimmers, W.J. ; Faber, J. ; Stone, D. ; Martins da Silva, P. ; Carvalho, F. ; Schmelz, R. ; Griffiths, B.S. ; Francisco, R. ; Creamer, R.E. ; Sousa, J.P. ; Bolger, T. - \ 2016
Applied Soil Ecology 97 (2016). - ISSN 0929-1393 - p. 86 - 97.
Cross-taxon congruence - Mites - Soil biodiversity assessment

The sustainable use of soils requires the protection of soil biodiversity because of its importance in the delivery of ecosystems services. However, no effective indicator exists which would allow assessment of the current state of biodiversity and is sensitive to change. This study, which is a component of the EcoFINDERS project, examines the use of mites (Acari) as a possible biological indicator of soil community composition. Thirty-six sites were sampled across 10 European countries spanning four bio-climatic zones (Alpine, Atlantic, Continental and Mediterranean) and 3 land uses (arable, grassland and forestry) for both biotic and abiotic variables. Results show a significant effect of bio-climatic zone on mite communities; in particular, the Mediterranean region had a rather distinct composition. Land use type significantly affected mite community composition and there was a distinct association with forestry. Cross-taxon congruence among soil taxa was variable and generally weak. Procrustes analysis showed that there was little similarity between the patterns of variation in mite community composition and those of other taxonomic groups (Collembola, Enchytraeidae, Nematoda and microbes). Mite and Collembola communities had the strongest correlation ( r= 0.4316, p

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