THE MICROBIAL REGULATION OF GLOBAL BIOGEOCHEMICAL CYCLES Topic Editors Johannes Rousk and Per Bengtson MICROBIOLOGY THE MICROBIAL REGULATION OF GLOBAL BIOGEOCHEMICAL CYCLES Topic Editors Johannes Rousk and Per Bengtson THE MICROBIAL REGULATION OF GLOBAL BIOGEOCHEMICAL CYCLES Topic Editors Johannes Rousk and Per Bengtson THE MICROBIAL REGULATION OF GLOBAL BIOGEOCHEMICAL CYCLES Topic Editors Johannes Rousk and Per Bengtson Frontiers in Microbiology October 2014 | The Microbial Regulation of Global Biogeochemical Cycles | 1 ABOUT FRONTIERS Frontiers is more than just an open-access publisher of scholarly articles: it is a pioneering approach to the world of academia, radically improving the way scholarly research is managed. The grand vision of Frontiers is a world where all people have an equal opportunity to seek, share and generate knowledge. Frontiers provides immediate and permanent online open access to all its publications, but this alone is not enough to realize our grand goals. FRONTIERS JOURNAL SERIES The Frontiers Journal Series is a multi-tier and interdisciplinary set of open-access, online journals, promising a paradigm shift from the current review, selection and dissemination processes in academic publishing. All Frontiers journals are driven by researchers for researchers; therefore, they constitute a service to the scholarly community. At the same time, the Frontiers Journal Series operates on a revo- lutionary invention, the tiered publishing system, initially addressing specific communities of scholars, and gradually climbing up to broader public understanding, thus serving the interests of the lay society, too. DEDICATION TO QUALITY Each Frontiers article is a landmark of the highest quality, thanks to genuinely collaborative interac- tions between authors and review editors, who include some of the world’s best academicians. Research must be certified by peers before entering a stream of knowledge that may eventually reach the public - and shape society; therefore, Frontiers only applies the most rigorous and unbiased reviews. Frontiers revolutionizes research publishing by freely delivering the most outstanding research, evaluated with no bias from both the academic and social point of view. By applying the most advanced information technologies, Frontiers is catapulting scholarly publishing into a new generation. WHAT ARE FRONTIERS RESEARCH TOPICS? Frontiers Research Topics are very popular trademarks of the Frontiers Journals Series: they are collections of at least ten articles, all centered on a particular subject. With their unique mix of varied contributions from Original Research to Review Articles, Frontiers Research Topics unify the most influential researchers, the latest key findings and historical advances in a hot research area! Find out more on how to host your own Frontiers Research Topic or contribute to one as an author by contacting the Frontiers Editorial Office: researchtopics@frontiersin.org FRONTIERS COPYRIGHT STATEMENT © Copyright 2007-2014 Frontiers Media SA. All rights reserved. All content included on this site, such as text, graphics, logos, button icons, images, video/audio clips, downloads, data compilations and software, is the property of or is licensed to Frontiers Media SA (“Frontiers”) or its licensees and/or subcontractors. The copyright in the text of individual articles is the property of their respective authors, subject to a license granted to Frontiers. The compilation of articles constituting this e-book, wherever published, as well as the compilation of all other content on this site, is the exclusive property of Frontiers. For the conditions for downloading and copying of e-books from Frontiers’ website, please see the Terms for Website Use. If purchasing Frontiers e-books from other websites or sources, the conditions of the website concerned apply. Images and graphics not forming part of user-contributed materials may not be downloaded or copied without permission. Individual articles may be downloaded and reproduced in accordance with the principles of the CC-BY licence subject to any copyright or other notices. They may not be re-sold as an e-book. As author or other contributor you grant a CC-BY licence to others to reproduce your articles, including any graphics and third-party materials supplied by you, in accordance with the Conditions for Website Use and subject to any copyright notices which you include in connection with your articles and materials. All copyright, and all rights therein, are protected by national and international copyright laws. The above represents a summary only. For the full conditions see the Conditions for Authors and the Conditions for Website Use. ISSN 1664-8714 ISBN 978-2-88919-297-7 DOI 10.3389/978-2-88919-297-7 Frontiers in Microbiology October 2014 | The Microbial Regulation of Global Biogeochemical Cycles | 2 THE MICROBIAL REGULATION OF GLOBAL BIOGEOCHEMICAL CYCLES Earth - the scene for the microbial regulation of biogeochemical cycles. Credit: Visible Earth, NASA. Image by: Stöckli, Nelson, Hasler. Laboratory for Atmospheres, Goddard Space Flight Center http://rsd. gsfc.nasa.gov/rsd Topic Editors: Johannes Rousk, Lund University, Sweden Per Bengtson, Lund University, Sweden Frontiers in Microbiology October 2014 | The Microbial Regulation of Global Biogeochemical Cycles | 3 Global biogeochemical cycles of carbon and nutrients are increasingly affected by human activities. So far, modeling has been central for our understanding of how this will affect ecosystem functioning and the biogeochemical cycling of carbon and nutrients. These models have been forced to adopt a reductive approach built on the flow of carbon and nutrients between pools that are difficult or even impossible to verify with empirical evidence. Furthermore, while some of these models include the response in physiology, ecology and biogeography of primary producers to environmental change, the microbial part of the ecosystem is generally poorly represented or lacking altogether. The principal pool of carbon and nutrients in soil is the organic matter. The turnover of this reservoir is governed by microorganisms that act as catalytic converters of environmental conditions into biogeochemical cycling of carbon and nutrients. The dependency of this conversion activity on individual environmental conditions such as pH, moisture and temperature has been frequently studied. On the contrary, only rarely have the microorganisms involved in carrying out the processes been identified, and one of the biggest challenges for advancing our understanding of biogeochemical processes is to identify the microorganisms carrying out a specific set of metabolic processes and how they partition their carbon and nutrient use. We also need to identify the factors governing these activities and if they result in feedback mechanisms that alter the growth, activity and interaction between primary producers and microorganisms. By determining how different groups of microorganisms respond to individual environmental conditions by allocating carbon and nutrients to production of biomass, CO 2 and other products, a mechanistic as well as quantitative understanding of formation and decomposition of organic matter, and the production and consumption of greenhouse gases, can be achieved. In this Research Topic, supported by the Swedish research councils’ programme “Biodiversity and Ecosystem Services in a Changing Landscape” (BECC), we intend to promote this alternative framework to address how cycling of carbon and nutrients will be altered in a changing environment from the first-principle mechanisms that drive them – namely the ecology, physiology and biogeography of microorganisms – and on up to emerging global biogeochemical patterns. This novel and unconventional approach has the potential to generate fresh insights that can open up new horizons and stimulate rapid conceptual development in our basic understanding of the regulating factors for global biogeochemical cycles. The vision for the research topic is to facilitate such progress by bringing together leading scientists as proponents of several disciplines. By bridging Microbial Ecology and Biogeochemistry, connecting microbial activities at the micro-scale to carbon fluxes at the ecosystem-scale, and linking above- and belowground ecosystem functioning, we can leap forward from the current understanding of the global biogeochemical cycles. Frontiers in Microbiology October 2014 | The Microbial Regulation of Global Biogeochemical Cycles | 4 Table of Contents 06 Microbial Regulation of Global Biogeochemical Cycles Johannes Rousk and Per Bengtson 09 Bacterial Chitin Degradation—Mechanisms and Ecophysiological Strategies Sara Beier and Stefan Bertilsson 21 Field and Lab Conditions Alter Microbial Enzyme and Biomass Dynamics Driving Decomposition of the Same Leaf Litter Zachary L. Rinkes, Robert L. Sinsabaugh, Daryl L. Moorhead, A. Stuart Grandy and Michael N. Weintraub 35 Dynamic Relationships Between Microbial Biomass, Respiration, Inorganic Nutrients and Enzyme Activities: Informing Enzyme-Based Decomposition Models D. L. Moorhead, Z. L. Rinkes, R. L. Sinsabaugh and M. N. Weintraub 47 Environmental impacts on the Diversity of Methane-Cycling Microbes and their Resultant Function Emma L. Aronson, Steven D. Allison and Brent R. Helliker 62 Controls on Bacterial and Archaeal Community Structure and Greenhouse Gas Production in Natural, Mined, and Restored Canadian Peatlands Nathan Basiliko, Kevin Henry, Varun Gupta, Tim R. Moore, Brian T. Driscoll and Peter F . Dunfield 76 Metabolic Adaptation and Trophic Strategies of Soil Bacteria—C1- Metabolism and Sulfur Chemolithotrophy in Starkeya Novella Ulrike Kappler and Amanda S. Nouwens 88 A Meta-Analysis of Soil Microbial Biomass Responses to Forest Disturbances Sandra R. Holden and Kathleen K. Treseder 105 Microbial Responses to Multi-Factor Climate Change: Effects on Soil Enzymes J. Megan Steinweg, Jeffrey S. Dukes, Eldor A. Paul and Matthew D. Wallenstein 116 Thermal Adaptation of Decomposer Communities in Warming Soils Mark A. Bradford 132 Controls on Soil Microbial Community Stability Under Climate Change Franciska T. de Vries and Ashley Shade 148 Plant Soil Interactions Alter Carbon Cycling in an Upland Grassland Soil Bruce C. Thomson, NIck J. Ostle, Niall P . McNamara, Simon Oakley, Andrew S. Whiteley, Mark J. Bailey and Robert I. Griffiths 160 Off-Season Biogenic Volatile Organic Compound Emissions From Heath Mesocosms: Responses to Vegetation Cutting Riikka Rinnan, Diana Gierth, Merete Bilde, Thomas Rosenørn and Anders Michelsen Frontiers in Microbiology October 2014 | The Microbial Regulation of Global Biogeochemical Cycles | 5 170 Effects of Spartina Alterniflora Invasion on the Communities of Methanogens and Sulfate-Reducing Bacteria in Estuarine Marsh Sediments Jemaneh Zeleke, Qiang Sheng, Jian-Gong Wang, Ming-Yao Huang, Fei Xia, Ji-Hua Wu and Zhe-Xue Quan 183 Rhizosphere Priming: A Nutrient Perspective Feike A. Dijkstra, Yolima Carrillo, Elise Pendall and Jack A. Morgan 191 Stoichiometric Imbalances Between Terrestrial Decomposer Communities and their Resources: Mechanisms and Implications of Microbial Adaptations to their Resources Maria Mooshammer, Wolfgang Wanek, Sophie Zechmeister-Boltenstern and Andreas Anatol Richter 201 Moss-Cyanobacteria Associations as Biogenic Sources of Nitrogen in Boreal Forest Ecosystems Kathrin Rousk, Davey L. Jones and Thomas H. DeLuca 211 Microbes in Nature are Limited by Carbon and Energy: The Starving-Survival Lifestyle in Soil and Consequences for Estimating Microbial Rates John E. Hobbie and Erik A. Hobbie 222 Specificity of Plant-Microbe Interactions in the Tree Mycorrhizosphere Biome and Consequences for Soil C Cycling Carolyn Churchland and Sue J. Grayston EDITORIAL published: 14 March 2014 doi: 10.3389/fmicb.2014.00103 Microbial regulation of global biogeochemical cycles Johannes Rousk* and Per Bengtson Department of Biology/Microbial Ecology, Lund University, Lund, Sweden *Correspondence: johannes.rousk@biol.lu.se Edited by: Lisa Y. Stein, University of Alberta, Canada Reviewed by: Pierre Offre, University of Vienna, Austria Keywords: microbial ecology, biogeochemistry, stoichiometry, climate change, soil microbiology, elemental fluxes, respiration, aquatic microbiology Global biogeochemical cycles of carbon and other nutrients are increasingly affected by human activities (Griggs et al., 2013). So far, modeling has been central for our understanding of how this will affect ecosystem functioning and the biogeochemical cycling of elements (Treseder et al., 2012). These models adopt a reduc- tive approach built on the flow of elements between pools that are difficult or even impossible to verify with empirical evidence. Furthermore, while some of these models include the response in physiology, ecology and biogeography of primary producers to environmental change, the microbial part of the ecosystem is gen- erally poorly represented or lacking altogether (Stein and Nicol, 2011; Treseder et al., 2012). The principal pool of carbon and other nutrients in soil is the organic matter (Schimel, 1995). The turnover time of this reservoir is governed by the rate at which microorganisms con- sume it. The rate of organic matter degradation in a soil is determined by both the indigenous microbial community and the environmental conditions (e.g., temperature, pH, soil water capacity, etc.), which govern the biogeochemical activities of the microorganisms (Waksman and Gerretsen, 1931; Schmidt et al., 2011). The dependences of these biogeochemical activity rates on environmental conditions such as pH, moisture and temper- ature have been frequently studied (Conant et al., 2011; Schmidt et al., 2011). However, while various microorganisms involved in carrying out biogeochemical processes have been identified, bio- geochemical process rates are only rarely measured together with microbial growth, and one of the biggest challenges for advancing our understanding of biogeochemical processes is to system- atically link biogeochemistry to the rate of specific metabolic processes (Rousk and Bååth, 2011; Stein and Nicol, 2011). We also need to identify the factors governing these activities and if it results in feedback mechanisms that alter the growth, activity and interaction between primary producers and microorgan- isms (Treseder et al., 2012). By determining how different groups of microorganisms respond to individual environmental condi- tions by allocating e.g. carbon to production of biomass, CO 2 and other products, a mechanistic as well as quantitative under- standing of formation and decomposition of organic matter, and the production and consumption of greenhouse gases, can be achieved. In this Research Topic, supported by the Swedish research councils’ program “Biodiversity and Ecosystem Services in a Changing Landscape” (BECC), we intend to promote an alternative framework to address how cycling of carbon and other nutrients will be altered in a changing environment from the first-principle mechanisms that drive them—namely the ecol- ogy, physiology and biogeography of microorganisms. In order to improve the predictive power of current models, the alternative framework supports the development of new models of biogeo- chemical cycles that factor in microbial physiology, ecology, and biogeochemistry. Our ambition has been richly rewarded by an extensive list of submissions. We are pleased to present contribu- tions including primary research targeting the microbial control of biogeochemistry, comprehensive reviews of how microbial processes and communities relate to biogeochemical cycles, iden- tification of critical challenges that remain, and new perspectives and ideas of how to optimize progress in our understanding of the microbial regulation of biogeochemistry. Our Research Topic presents new findings about the impor- tance of the microbial community composition, their metabolic state, and the activity of enzymes for the fate and degradation of specific substrates such as chitin (Beier and Bertilsson, 2013), the degradation of more complex compounds such as those consti- tuting plant litter (Moorhead et al., 2013; Rinkes et al., 2013), and the metabolism and biogeochemical cycling of one-carbon compounds (Aronson et al., 2013; Basiliko et al., 2013; Kappler and Nouwens, 2013). The environmental control and land-use perturbation of microbial communities and methane produc- tion were assessed in a comprehensive review (Aronson et al., 2013) as well as a case study (Basiliko et al., 2013) and a meta- analysis (Holden and Treseder, 2013). Other contributions have focused on how environmental variables that are affected by climate change can modulate microbial activities by e.g. their influence on the production and activity of enzymes (Steinweg et al., 2013), while Bradford (2013) has provided a comprehensive review of how microbial processes respond to warmer tempera- tures. These reviews are accompanied by a new suggestion for how we can achieve better predictions for microbial responses (and feedbacks) to climate change (de Vries and Shade, 2013), while Moorhead et al. (2013) identify knowledge gaps and provide important insights about how data on microbial communities, environmental conditions, and enzyme activities can be used to better inform enzyme-based models. Several submissions have highlighted the importance for plant-microbial feedbacks for the regulation of organic matter decomposition and formation (Moorhead et al., 2013; Thomson www.frontiersin.org March 2014 | Volume 5 | Article 103 | 6 Rousk and Bengtson Microbial regulation of global biogeochemical cycles et al., 2013; Churchland and Grayston, under review), the produc- tion of biogenic volatile organic compounds (Rinnan et al., 2013), and the community composition of methanogens and sulfate reducing bacteria (Zeleke et al., 2013). A very active research area in soil microbial ecology is presently how small amounts of labile carbon sources can trigger, or “prime,” the decomposition of soil organic matter. A route toward a more general understanding of the regulation of plant-soil interaction for biogeochemistry, that may well facilitate our understanding of “priming effects,” could be the incorporation of stoichiometric concepts (Dijkstra et al., 2013; Mooshammer et al., 2014). Stoichiometric variations in the concentration of nutrients, combined with variations in carbon and nutrient demands of different decomposer groups, also seems to be reflected in the degradation rate of plant litter (Rinkes et al., 2013). A comprehensive review of biogenic fixation of nitrogen demonstrates the importance of interactions between different biogeochemical cycles for nitrogen fixation in ecosystems with nitrogen-limited plant productivity (Rousk et al., 2013). These contributions emphasize that stoichiometric variations in nutri- ent concentrations are of importance for both factors that could determine the propensity for organic matter to accumulate in an ecosystem, and thus for carbon to be sequestered. Some contributions to this Research Topic have also high- lighted methodological challenges that urgently need attention. For instance, the ability of contemporary isotopic tracer meth- ods to estimate microbial contributions to biogeochemical pro- cesses could be systematically overestimated (Hobbie and Hobbie, 2013), suggesting that estimates of the turnover of low molecular weight organic compounds, and possibly also for estimations of nitrogen transformation rates, need to be revised. Additionally, there is a need to move from laboratory-based estimations of the microbial role in ecosystem level processes, often omitting cru- cial components such as the presence of plants, to field-based assessments in intact systems (Rinkes et al., 2013). The contributions to our Research Topic have opened up new horizons and stimulated conceptual developments in our basic understanding of the regulating factors of global biogeochemi- cal cycles. Within this forum, we have begun to bridge Microbial Ecology and Biogeochemistry, connecting microbial activities at the microcosm scale to carbon fluxes at the ecosystem-scale, and linking above- and belowground ecosystem functioning. We are hopeful that we have initiated conceptual developments that can reach far beyond this Research Topic. It is a mere first step, but we are confident it is directed toward a predictive under- standing of the microbial regulation of global biogeochemical cycles. ACKNOWLEDGMENTS This Research Topic was supported by the action-group “MICROGLOBE” within the “Biodiversity and Ecosystem Services in a Changing Landscape” (BECC) environment funded by the Swedish Research Council. We are grateful to the Frontiers team support and editorial endorsement of our ambitions. REFERENCES Aronson, E. L., Allison, S. D., and Helliker, B. R. (2013). Environmental impacts on the diversity of methane-cycling microbes and their resultant function. Front. Microbiol . 4:225. doi: 10.3389/fmicb.2013.00225 Basiliko, N., Henry, K., Gupta, V., Moore, T. R., Driscoll, B. T., and Dunfield, P. F. (2013). Controls on bacterial and archaeal community structure and green- house gas production in natural, mined, and restored Canadian peatlands. Front. Microbiol . 4:215. doi: 10.3389/fmicb.2013.00215 Beier, S., and Bertilsson, S. (2013). Bacterial chitin degradation— mechanisms and ecophysiological strategies. Front. Microbiol 4:149. doi: 10.3389/fmicb.2013.00149 Bradford, M. A. (2013). Thermal adaptation of decomposer communities in warming soils. Front. Microbiol . 4:333. doi: 10.3389/fmicb.2013.00333 Conant, R. T., Ryan, M. G., Ågren, G. I., Birge, H. E., Davidson, E. A., Eliasson, P. E., et al. (2011). Temperature and soil organic matter decomposition rates - synthe- sis of current knowledge and a way forward. Global Change Biol . 17, 3392–3404. doi: 10.1111/j.1365-2486.2011.02496.x de Vries, F. T., and Shade, A. (2013). Controls on soil microbial community stability under climate change. Front. Microbiol . 4:265. doi: 10.3389/fmicb.2013.00265 Dijkstra, F. A., Carrillo, Y., Pendall, E., and Morgan, J. A. (2013). Rhizosphere priming: a nutrient perspective. Front. Microbiol . 4:216. doi: 10.3389/fmicb.2013.00216 Griggs, D., Stafford-Smith, M., Gaffney, O., Rockström, J., Öhman, M. C., Shyamsundar, P., et al. (2013). Sustainable development goals for people and planet. Nature 495, 305–307. doi: 10.1038/495305a Hobbie, J. E., and Hobbie, E. A. (2013). Microbes in nature are limited by carbon and energy: the starving-survival lifestyle in soil and consequences for estimat- ing microbial rates. Front. Microbiol . 4:324. doi: 10.3389/fmicb.2013.00324 Holden, S. R., and Treseder, K. K. (2013). A meta-analysis of soil micro- bial biomass responses to forest disturbances. Front. Microbiol . 4:163. doi: 10.3389/fmicb.2013.00163 Kappler, U., and Nouwens, A. S. (2013). Metabolic adaptation and trophic strate- gies of soil bacteria—C1- metabolism and sulfur chemolithotrophy in Starkeya novella. Front. Microbiol . 4:304. doi: 10.3389/fmicb.2013.00304 Moorhead, D. L., Rinkes, Z. L., Sinsabaugh, R. L., and Weintraub, M. N. (2013). Dynamic relationships between microbial biomass, respiration, inorganic nutri- ents and enzyme activities: informing enzyme-based decomposition models. Front. Microbiol . 4:223. doi: 10.3389/fmicb.2013.00223 Mooshammer, M., Wanek, W., Zechmeister-Boltenstern, S., and Richter, A. A. (2014). Stoichiometric imbalances between terrestrial decomposer commu- nities and their resources: mechanisms and implications of microbial adap- tations to their resources. Front. Microbiol . 5:22. doi: 10.3389/fmicb.2014. 00022 Rinkes, Z. L., Sinsabaugh, R. L., Moorhead, D. L., Grandy, A. S., and Weintraub, M. N. (2013). Field and lab conditions alter microbial enzyme and biomass dynam- ics driving decomposition of the same leaf litter. Front. Microbiol . 4:260. doi: 10.3389/fmicb.2013.00260 Rinnan, R., Gierth, D., Bilde, M., Rosenørn, T., and Michelsen, A. (2013). Off-season biogenic volatile organic compound emissions from heath mesocosms: responses to vegetation cutting. Front. Microbiol . 4:224. doi: 10.3389/fmicb.2013.00224 Rousk, J., and Bååth, E. (2011). Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiol. Ecol. 78, 17–30. doi: 10.1111/j.1574-6941.2011.01106.x Rousk, K., Jones, D. L., and DeLuca, T. H. (2013). Moss-cyanobacteria associations as biogenic sources of nitrogen in boreal forest ecosystems. Front. Microbiol 4:150. doi: 10.3389/fmicb.2013.00150 Schimel, D. S. (1995). Terrestrial ecosystems and the carbon-cycle. Global Change Biol . 1, 77–91. doi: 10.1111/j.1365-2486.1995.tb00008.x Schmidt, M. W. I., Torn, M. S., Abiven, S., Dittmar, T., Guggenberger, G., Janssens, I. A., et al. (2011). Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56. doi: 10.1038/nature10386 Stein, L. Y., and Nicol, W. N. (2011). Grand challenges in terrestrial microbiology. Front. Microbiol . 2:6. doi: 10.3389/fmicb.2011.00006 Steinweg, J. M., Dukes, J. S., Paul, E. A., and Wallenstein, M. D. (2013). Microbial responses to multi-factor climate change: effects on soil enzymes. Front. Microbiol . 4:146. doi: 10.3389/fmicb.2013.00146 Thomson, B. C., Ostle, N. J., McNamara, N. P., Oakley, S., Whiteley, A. S., Bailey, M. J., et al. (2013). Plant soil interactions alter carbon cycling in an upland grassland soil. Front. Microbiol . 4:253. doi: 10.3389/fmicb.2013.00253 Treseder, K. K., Balser, T. C., Bradford, M. A., Brodie, E. L., Dubinsky, E. A., Eviner, V. T., et al. (2012). Integrating microbial ecology into ecosystem models: challenges and priorities. Biogeochemistry 109, 7–18. doi: 10.1007/s10533-011- 9636-5 Frontiers in Microbiology | Terrestrial Microbiology March 2014 | Volume 5 | Article 103 | 7 Rousk and Bengtson Microbial regulation of global biogeochemical cycles Waksman, S. A., and Gerretsen, F. C. (1931). Influence of temperature and moisture upon the nature and extent of decompositiion of plant residues by microorganisms. Ecology 12, 33–60 Zeleke, J., Sheng, Q., Wang, J.-G., Huang, M.-Y., Xia, F., Wu J-H., and Quan, Z. (2013). Effects of Spartina alterniflora invasion on the communities of methanogens and sulfate-reducing bacteria in estuarine marsh sediments. Front. Microbiol . 4:243. doi: 10.3389/fmicb.2013.00243 Received: 11 February 2014; accepted: 27 February 2014; published online: 14 March 2014. Citation: Rousk J and Bengtson P (2014) Microbial regulation of global biogeochemical cycles. Front. Microbiol. 5 :103. doi: 10.3389/fmicb.2014.00103 This article was submitted to Terrestrial Microbiology, a section of the journal Frontiers in Microbiology. Copyright © 2014 Rousk and Bengtson. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, dis- tribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. www.frontiersin.org March 2014 | Volume 5 | Article 103 | 8 REVIEW ARTICLE published: 14 June 2013 doi: 10.3389/fmicb.2013.00149 Bacterial chitin degradation—mechanisms and ecophysiological strategies Sara Beier 1,2,3 and Stefan Bertilsson 1 * 1 Department of Ecology and Genetics, Limnology, Uppsala University, Uppsala, Sweden 2 Laboratoire d’OcØanographie Microbienne, Observatoire OcØanologique, UPMC Paris 06, UMR 7621, Banyuls sur mer, France 3 Laboratoire d’OcØanographie Microbienne, Observatoire OcØanologique Centre National de la Recherche Scientifique, UMR 7621, Banyuls sur mer, France Edited by: Per Bengtson, Lund University, Sweden Reviewed by: Steffen Kolb, University of Bayreuth, Germany Helmut Buergmann, Eawag: Swiss Federal Institute of Aquatic Science and Technology, Switzerland *Correspondence: Stefan Bertilsson, Department of Ecology and Genetics, Limnology, Uppsala University, Norbyv. 18D, SE-75236 Uppsala, Sweden e-mail: stebe@ebc.uu.se Chitin is one the most abundant polymers in nature and interacts with both carbon and nitrogen cycles. Processes controlling chitin degradation are summarized in reviews published some 20 years ago, but the recent use of culture-independent molecular methods has led to a revised understanding of the ecology and biochemistry of this process and the organisms involved. This review summarizes different mechanisms and the principal steps involved in chitin degradation at a molecular level while also discussing the coupling of community composition to measured chitin hydrolysis activities and substrate uptake. Ecological consequences are then highlighted and discussed with a focus on the cross feeding associated with the different habitats that arise because of the need for extracellular hydrolysis of the chitin polymer prior to metabolic use. Principal environmental drivers of chitin degradation are identified which are likely to influence both community composition of chitin degrading bacteria and measured chitin hydrolysis activities. Keywords: chitin, particles, organic matter, bacteria, interactions, cross-feeding, glycoside hydrolase INTRODUCTION The occurrence of chitin is widespread in nature and chitin serves as a structural element in many organisms, e.g., fungi, crus- taceans, insects or algae (Gooday, 1990a,b). Chitin is composed of linked amino sugar subunits. Similar to cellulose and murein, it makes a shortlist of highly abundant biopolymers with enormous global production rates estimated at approximately 10 10 –10 11 tons year − 1 (Gooday, 1990a; Whitman et al., 1998; Kaiser and Benner, 2008). There are no reports of quantitatively significant long-term accumulation of chitin in nature, implying efficient degradation and turnover (Tracey, 1957; Gooday, 1990a). In accordance with the abundance and ubiquity of chitin, chitin-degrading enzymes are also detected in many types of organisms, such as fungi, bacteria (Gooday, 1990a), archaea (Huber et al., 1995; Tanaka et al., 1999; Gao et al., 2003), rotifers (Štrojsová and Vrba, 2005), some algae (Vrba et al., 1996; Štrojsová and Dyhrman, 2008), but also carnivorous plants or in digestional tracts of higher animals (Gooday, 1990a). Bacteria are believed to be major mediators of chitin degrada- tion in nature. In soil systems, chitin hydrolysis rates have been shown to correlate with bacterial abundance (Kielak et al., 2013), but depending on temperature, pH, or the successional stage of the degradation process, also fungi may be quantitatively impor- tant agents of chitin degradation (Gooday, 1990a; Hallmann et al., 1999; Manucharova et al., 2011). In aquatic systems, plating and in situ colonization experiments convincingly demonstrates that bacteria are the main mediators of chitin degradation (Aumen, 1980; Gooday, 1990a). However, occasionally, dense fungal colo- nization of chitinous zooplankton carapaces has been observed (Wurzbacher et al., 2010) and some diatoms have also been shown to hydrolyze chitin oligomers (Vrba et al., 1996, 1997). A further source of chitin modifying enzymes in aquatic systems are enzymes released during molting of planktonic crustaceans (Vrba and Machacek, 1994). Nevertheless, it is not yet clear whether the enzymes released by diatoms and molting zooplankton react with particulate chitin to any significant extent or if their hydrolytic activity is limited to dissolved chitin oligomers. Chitin is the polymer of (1 → 4)- β -linked N-acetyl-D- glucosamine (GlcNAc). The single sugar units are rotated 180 ◦ to each other with the disaccharide N,N ÷ -diacetylchitobiose [(GlcNAc) 2 ] as the structural subunit. In nature, chitin varies in the degree of deacetylation and therefore the distinction from chitosan, which is the completely deacetylated form of the poly- mer, is not strict. Chitin is classified into three different crystalline forms: the α -, β -, and γ -form, which differ in the orientation of chitin micro-fibrils. With few exceptions, natural chitin occurs associated to other structural polymers such as proteins or glu- cans, which often contribute more than 50% of the mass in chitin-containing tissue (Attwood and Zola, 1967; Schaefer et al., 1987; Merzendorfer and Zimoch, 2003). Chitin is a structural homologue of cellulose where the latter is composed of glucose instead of GlcNAc subunits. Also murein in bacterial cell walls can be considered a structural chitin homologue, as it is composed of alternating (1 → 4)- β -linked GlcNAc and N-acetylmuramic acid units. A process is called chitinoclastic if chitin is degraded. If this degradation involves the initial hydrolysis of the (1 → 4)- β - glycoside bond, as seen for chitinase-catalyzed chitin degradation, the process is called chitinolytic. Growth on chitin is not nec- essarily accompanied by the direct dissolution of its polymeric www.frontiersin.org June 2013 | Volume 4 | Article 149 | 9 Beier and Bertilsson Bacterial chitin degradation structure. Alternatively, chitin can be deacetylated to chitosan or possibly even cellulose-like forms, if it is further subjected to deamination ( Figure 1 ). Such a degradation mechanism has been suggested in some early studies (ZoBell and Rittenberg, 1938; Campbell and Williams, 1951). Chitinases and chitosanases overlap in substrate specificity, while their respective efficiency is controlled by the degree of deacetylation of the polymeric sub- strate (Somashekar and Joseph, 1996) ( Figure 1 ). Besides specific chitosanases, also cellulases can possess considerable chitosan- cleaving activity (Xia et al., 2008). Furthermore, lysozyme has also been shown to hydrolyze chitin, even if processivity is low when compared to true chitinases (Skujin ̧ š et al., 1973). Cellulases can also bind directly to chitin (Ekborg et al., 2007; Li and Wilson, 2008), but there are no reports of these enzymes actually hydrolyzing the polymers. Few studies have compared the quantitative importance of different chitinoclastic pathways, and the studies available sug- gest that chitin degradation via initial deacetylation might be more important in soil and sediment compared to water envi- ronments (Hillman et al., 1989; Gooday, 1990a). The quantitative importance of different chitinoclastic pathways from a global per- spective has, to the best of our knowledge, never been assessed. In the following sections, we will focus on the chitinolytic pathway. The quantitative significance of chitin has been recognized for some time and there has been great interest in identifying pro- cesses and factors controlling its degradation. Accordingly, the biochemistry, molecular biology, and biogeochemistry of chitin degradation have been summarized in reviews published already some 20 years ago (Gooday, 1990a; Cohen-Kupiec and Chet, 1998; Keyhani and Roseman, 1999). More recently, the devel- opment and widespread use of culture-independent molecular methods in microbial ecology have enabled further dissection of microbial processes controlling chitin degradation in more com- plex natural environments and diverse microbial communities. These methodological advances combined with the significance of chitin as a critical link between the carbon and nitrogen cycles ( Figure 2 ) has led to a revived interest in the quantitative importance of chitin turnover in marine systems (Souza et al., 2011). There is clearly a need for an updated account of the diverse mechanisms involved in chitinolysis and the ecological con- sequences of this process for bacteria. A focus on bacteria rather than all other organisms involved in chitin degradation is warranted since bacterial chitin degradation takes place in all major ecosystems and because their metabolism and growth have such a central role in most ecosystem-scale biogeochemical FIGURE 1 | Processes involved in chitin degradation. If deacetylation and deamination processes are very active, chitosan or possibly even cellulose-like molecules might be produced. GH, glycoside hydrolase family; GlcNAc, N-acetylglucosamine; GlcN, glucosamine; Glc, glucose. Frontiers in Microbiology | Terrestrial Microbiology June 2013 | Volume 4 | Article 149 | 10 Beier and Bertilsson Bacterial chitin degradation FIGURE 2 | Fate of possible chitin degradation intermediates and degradation products at the interface of the global N and C-cycles: during the first degradation steps chitin is cleaved into small organic molecules that can directly be reintegrated into cell material or mineralized and potentially removed from the system. GlcNAc, N-acetylglucosamine; GlcN, glucosamine; Glc: glucose. cycles. However, also non-bacterial or non-chitinolytic chitin- degraders will occasionally be mentioned and discussed where their activities would influence bacterial chitin degradation. In light of recent developments in molecular methods, a particu- lar emphasis will be on how the participation and interactions of specific microbial populations and community composition influence the process. We further identify gaps in knowledge and needs for further research. BIOCHEMISTRY OF CHITIN HYDROLYSIS Chitin degradation is a highly regulated process, and the hydrolytic enzymes are induced by products of the chitin hydrol- yses, GlcNAc (Techkarnjanaruk et al., 1997), or soluble chitin oligomers (GlcNAc) 2 - 6 (Keyhani and Roseman, 1996; Miyashita et al., 2000; Li and Roseman, 2004; Meibom et al., 2004), depend- ing on the organism under scrutiny. In contrast to (GlcNAc) 2 , GlcNAc has also been reported to act as a suppressor of chiti- nase expression in a Streptomyces strain (Miyashita et al., 2000) and this may be because its main origin in natural systems could be from murein in cell walls rather than chitin (Benner and Kaiser, 2003). Other factors more generally regulating the expression of these and other hydrolytic enzymes are nutrient regime and availability of other, more readily available growth substrates (Techkarnjanaruk et al., 1997; Keyhani and Roseman, 1999; Delpin and Goodman, 2009a,b). The variety of regulating factors are likely to reflect the wide range of ecological niches occupied by chitin degraders. Complete lysis of the insoluble chitin polymer typically con- sists of three principal steps (1) cleaving the polymer into water- soluble oligomers, (2) splitting of these oligomers into dimers, and (3) cleavage of the dimers into monomers. The first two steps are usually catalyzed by chitinases. The occurrence of chiti- nases in bacteria is widespread among phyla and the production of multiple chitinolytic enzymes by individual bacterial strains appear to be a common trait (e.g., Fuchs et al., 1986; Romaguera et al., 1992; Saito et al., 1999; Shimosaka et al., 2001; Tsujibo et al., 2003). Chitinases are typically grouped into family 18 and 19 glycoside hydrolases. The latter are rare in bacteria except for some members of the genus Streptomyces (Ohno et al., 1996; Saito et al., 1999; Watanabe et al., 1999; Shimosaka et al., 2001; Tsujibo et al., 2003). It has been hypothesized that family 18 and 19 gly- coside hydrolases have evolved separately, as genes belonging to these two analogous gene families show little or no sequence homology, nor share the same molecular-level catalytic mech- anism (Perrakis et al., 1994; Davies and Henrissat, 1995; Hart et al., 1995). The occurrence of multiple genes in a single organ- ism may be the result of gene duplication or acquisition of genes from other organisms via lateral gene transfer (Hunt et al., 2008). In support of the former mechanism, different chitinase gene sequences found within single organisms are often almost identi- cal. However, there are ex