DOCSLIB.ORG

Syntrophic Exchange in Synthetic Microbial Communities PNAS PLUS

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Syntrophic Exchange in Synthetic Microbial Communities PNAS PLUS Syntrophic exchange in synthetic microbial communities PNAS PLUS Michael T. Meea,b, James J. Collinsa,c,d,e, George M. Churchb,c,1, and Harris H. Wangf,1 aDepartment of Biomedical Engineering, Boston University, Boston, MA 02215; bDepartment of Genetics, Harvard Medical School, Boston, MA 02115; cWyss Institute for Biologically Inspired Engineering, Harvard University, Boston, MA 02115; dHoward Hughes Medical Institute and eCenter of Synthetic Biology, Boston University, Boston, MA 02215; and fDepartment of Systems Biology, Columbia University, New York, NY 10032 Contributed by George M. Church, April 1, 2014 (sent for review January 30, 2014) Metabolic crossfeeding is an important process that can broadly amino acids in natural interkingdom and interspecies exchange shape microbial communities. However, little is known about networks (9–11). Recent comparative analyses of microbial specific crossfeeding principles that drive the formation and genomes suggest that a significant proportion of all bacteria lack maintenance of individuals within a mixed population. Here, we essential pathways for amino acid biosynthesis (2). These auxo- devised a series of synthetic syntrophic communities to probe the trophic microbes thus require extracellular sources of amino complex interactions underlying metabolic exchange of amino acids. acids for survival. Understanding amino acid exchange therefore We experimentally analyzed multimember, multidimensional com- presents an opportunity to gain new insights into basic principles munities of Escherichia coli of increasing sophistication to assess the in metabolic crossfeeding. Recently, several studies have used outcomes of synergistic crossfeeding. We find that biosynthetically model systems of Saccharomyces cerevisiae (12), Saccharomyces costly amino acids including methionine, lysine, isoleucine, arginine, enterica (13), and E. coli (14–16) to study syntrophic growth of and aromatics, tend to promote stronger cooperative interactions amino acid auxotrophs in coculture environments. Numerous than amino acids that are cheaper to produce. Furthermore, cells that quantitative models have also been developed to describe the share common intermediates along branching pathways yielded behavior of these multispecies systems, including those that in- more synergistic growth, but exhibited many instances of both pos- tegrate dynamics (17, 18), metabolism (19–21), and spatial co- itive and negative epistasis when these interactions scaled to higher ordination (22). Although these efforts have led to an improved dimensions. In more complex communities, we find certain members understanding of the dynamics of syntrophic pairs and the en- exhibiting keystone species-like behavior that drastically impact ergetic and benefits of cooperativity in these simple systems (23), the community dynamics. Based on comparative genomic analysis larger more complex syntrophic systems have yet to be explored. of >6,000 sequenced bacteria from diverse environments, we present SYSTEMS BIOLOGY Here, we use engineered E. coli mutants to study syntrophic evidence suggesting that amino acid biosynthesis has been broadly crossfeeding, scaling to higher-dimensional synthetic ecosystems optimized to reduce individual metabolic burden in favor of en- hanced crossfeeding to support synergistic growth across the bio- of increasing sophistication. We first devised pairwise syntrophic sphere. These results improve our basic understanding of microbial communities that show essential and interesting dynamics that syntrophy while also highlighting the utility and limitations of cur- can be predicted by simple kinetic models. We then increased rent modeling approaches to describe the dynamic complexities un- the complexity of the interaction in three-member synthetic derlying microbial ecosystems. This work sets the foundation for consortia involving crossfeeding of multiple metabolites. To future endeavors to resolve key questions in microbial ecology and further increase the complexity of our system, we devised a 14- evolution, and presents a platform to develop better and more ro- member community to understand key drivers of population dy- bust engineered synthetic communities for industrial biotechnology. namics over short and evolutionary timescales. Finally, we provide evidence for widespread trends of metabolic crossfeeding based synthetic ecosystem | amino acid exchange | population modeling on comparative genomic analysis of aminoacidbiosynthesisacross icrobes are abundantly found in almost every part of the Significance Mworld, living in communities that are diverse in many facets. Although it is clear that cooperation and competition Metabolic exchange between microbes is a crucial process within microbial communities is central to their stability, main- driving the development of microbial ecosystems. The ex- tenance, and longevity, there is limited knowledge about the change of essential amino acids presents an opportunity to general principles guiding the formation of these intricate sys- investigate the guiding principles underlying microbial trade in tems. Understanding the underlying governing principles that nature. In this study, we devised synthetic communities of shape a microbial community is key for microbial ecology but is Escherichia coli bacteria of increasing complexity to measure also crucial for engineering synthetic microbiomes for various general properties enabling metabolic exchange of amino acids. biotechnological applications (1–3). Numerous such examples We identified numerous syntrophic interactions that enable co- have been recently described including the bioconversion of operative growth, which exhibited both positive and negative unprocessed cellulolytic feedstocks into biofuel isobutanol using epistasis with increasing community complexity. Our results fungal–bacterial communities (4) and biofuel precursor methyl suggest that amino acid auxotrophy may be an evolutionarily halides using yeast–bacterial cocultures (5). Other emerging optimizing strategy to reduce biosynthetic burden while pro- applications in biosensing and bioremediation against environ- moting cooperative interactions between different bacteria in mental toxins such as arsenic (6) and pathogens such as Pseu- the microbiome. domonas aeruginosa and Vibrio cholerae have been demonstrated using engineered quorum-sensing Escherichia coli (7, 8). These Author contributions: M.T.M., J.J.C., G.M.C., and H.H.W. designed research; M.T.M. and H.H.W. performed research; M.T.M. and H.H.W. contributed new reagents/analytic tools; advances paint an exciting future for the development of sophis- M.T.M. and H.H.W. analyzed data; and M.T.M., J.J.C., G.M.C., and H.H.W. wrote ticated multispecies microbial communities to address pressing the paper. challenges and the crucial need to understand the basic principles The authors declare no conflict of interest. that enables their design and engineering. Freely available online through the PNAS open access option. An important process that governs the growth and composi- 1To whom correspondence may be addressed. E-mail: [email protected] tion of microbial ecosystems is the exchange of essential or [email protected]. metabolites, known as metabolic crossfeeding. Entomological This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. studies have elucidated on a case-by-case basis the importance of 1073/pnas.1405641111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1405641111 PNAS | Published online April 28, 2014 | E2149–E2156 Downloaded by guest on September 28, 2021 thousands of sequenced genomes. Our large-scale and systematic glucose minimal media after 4 d and growth only when supple- efforts represent an important foray into forward and reverse en- mented with each amino acid needed. Using a microplate gineering synthetic microbial communities to gain key governing spectrophotometer, we performed kinetic growth curve analysis principles of microbial ecology and systems microbiology. for each of the 14 auxotrophs grown in M9-glucose supple- mented with varying initial amino acid levels. Under these amino Results acid-limiting conditions, an auxotrophic strain will grow expo- Our overall goal is to develop and understand a simple microbial nentially until the amino acid supplementation is exhausted (Fig. model of metabolic crossfeeding that can be scaled in a tractable S1B). Saturating cell densities (i.e., carrying capacities) plotted stepwise manner, toward reconstituting the complexity and dy- against initial seeding amino acid levels show a strong linear namics exhibited by natural ecosystems (Fig. 1A). To this end, we relationship (Fig. S1B) indicating that external amino acid levels devised a series of syntrophic microbial communities of in- can determine cell growth in a linear and predictable manner. creasing diversity and complexity using the simple model bacte- We estimated the number of extracellular amino acids needed to rium E. coli. Our system is based on the syntrophic behavior of generate a cell for each of the 14 amino acids (Fig. S1A and amino acid exchange between auxotrophic mutants to facilitate Dataset S1). The estimated biosynthetic cost to produce each coculture growth. We first investigated the energetics involved amino acid (24) shows a strong inverse relationship with the in amino acid utilization and exchange. Starting from a pro- amount of amino acids needed to produce a cell (Fig. 1B), totrophic E. coli
Load more

Recommended publications
  • The Syntrophy Hypothesis for the Origin of Eukaryotes Revisited Purificación López-García, David Moreira
    The Syntrophy hypothesis for the origin of eukaryotes revisited Purificación López-García, David Moreira To cite this version: Purificación López-García, David Moreira. The Syntrophy hypothesis for the origin of eukaryotes revisited. Nature Microbiology, Nature Publishing Group, 2020, 5 (5), pp.655-667. 10.1038/s41564- 020-0710-4. hal-02988531 HAL Id: hal-02988531 https://hal.archives-ouvertes.fr/hal-02988531 Submitted on 3 Dec 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. 1 2 Perspectives 3 4 5 6 The Syntrophy hypothesis for the origin of eukaryotes revisited 7 8 Purificación López-García1 and David Moreira1 9 10 1 Ecologie Systématique Evolution, CNRS, Université Paris-Saclay, AgroParisTech, Orsay, France 11 12 13 14 *Correspondence to: [email protected] 15 16 17 18 19 1 20 The discovery of Asgard archaea, phylogenetically closer to eukaryotes than other archaea, together with 21 improved knowledge of microbial ecology impose new constraints on emerging models for the origin of the 22 eukaryotic cell (eukaryogenesis). Long-held views are metamorphosing in favor of symbiogenetic models 23 based on metabolic interactions between archaea and bacteria. These include the classical Searcy’s and 24 hydrogen hypothesis, and the more recent Reverse Flow and Entangle-Engulf-Enslave (E3) models.
    [Show full text]
  • The Deep Continental Subsurface: the Dark Biosphere
    International Microbiology (2018) 21:3–14 https://doi.org/10.1007/s10123-018-0009-y REVIEW The deep continental subsurface: the dark biosphere Cristina Escudero1 & Mónica Oggerin1,2 & Ricardo Amils1,3 Received: 17 April 2018 /Revised: 8 May 2018 /Accepted: 9 May 2018 /Published online: 30 May 2018 # Springer International Publishing AG, part of Springer Nature 2018 Abstract Although information from devoted geomicrobiological drilling studies is limited, it is clear that the results obtained so far call for a systematic exploration of the deep continental subsurface, similar to what has been accomplished in recent years by the Ocean Drilling Initiatives. In addition to devoted drillings from the surface, much of the continental subsurface data has been obtained using different subterranean Bwindows,^ each with their correspondent limitations. In general, the number and diversity of microorganisms decrease with depth, and the abundance of Bacteria is superior to Archaea. Within Bacteria, the most commonly detected phyla correspond to Proteobacteria, Actinobacteria, Bacteroidetes, and Firmicutes. Within Archaea, methanogens are recurrently detected in most analyzed subsurface samples. One of the most controversial topics in the study of subsurface environments is whether the available energy source is endogenous or partly dependent on products photosynthetically generated in the subsurface. More information, at better depth resolution, is needed to build up the catalog of deep subsurface microbiota and the biologically available electron
    [Show full text]
  • Review: Short Chain Fatty Acids in Human Gut and Metabolic Health
    Wageningen Academic Beneficial Microbes, 2020; 11(5): 411-455 Publishers Short chain fatty acids in human gut and metabolic health E.E. Blaak1*, E.E. Canfora1, S. Theis2, G. Frost3, A.K. Groen4,5, G. Mithieux6, A. Nauta7, K. Scott8, B. Stahl9,10, J. van Harsselaar2, R. van Tol11, E.E. Vaughan12 and K. Verbeke13 1Department of Human Biology, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Universiteitssingel 50, 6229 ER Maastricht, The Netherlands.; 2Südzucker Group – Beneo, Wormser Str. 11, Mannheim, 67283, Germany; 3Faculty of Medicine, Department of Metabolism, Digestion and Reproduction, Imperial College London, SW7 2AZ London, United Kingdom; 4Diabetes Center, Department of Internal and Vascular Medicine, Amsterdam University Medical Centers, location AMC, Amsterdam, the Netherlands; 5Quantitative Systems Biology, Department of Pediatrics, Centre for Liver, Digestive and Metabolic Diseases, University Medical Centre Groningen (UMCG), University of Groningen, P.O. Box 30.001, 9700 RB Groningen, the Netherlands; 6INSERM U1213, Faculté de Médecine Laennec, University of Lyon, 7-11 Rue Guillaume Paradin, 69372 Lyon, France; 7FrieslandCampina, P.O. Box 1551, 3800 BN Amersfoort, the Netherlands; 8The Rowett Institute, University of Aberdeen, Aberdeen, AB25 2ZD, United Kingdom; 9Danone Nutricia Research, Uppsalalaan 12, 3584 CT, Utrecht, the Netherlands; 10Department of Chemical Biology & Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht University, Universiteitsweg 99, 3584
    [Show full text]
  • ENVIRONMENTAL MICROBIOLOGY Disentangling Syntrophy
    RESEARCH HIGHLIGHTS ENVIRONMENTAL MICROBIOLOGY Disentangling syntrophy Syntrophic interactions, in which direct electron transfer. These models intraspecies hydrogen transfer rather two or more microorganisms coop- were combined to provide an inte- than by DIET. Comparative analysis erate metabolically to metabolize grated genomic model of syntrophy, of the different modes of electron compounds that neither partner can introducing a shared metabolite pool transfer identified several factors that metabolize alone, are common in component to allow for the exchange influence which mode of transfer is environmental niches. Zengler and of metabolites both between species preferred, including the local avail- colleagues present a ‘multi-omics’, and with the external environment. ability of protons. systems-based workflow to investigate The electron transfer flux constraint Finally, the authors investigated the details of a syntrophic relationship was defined, which enabled DIET the adaptations that occured dur- between two Geobacter species. to be modelled. Physiological and ing syntrophic growth and found Syntrophy that involves interspe- transcriptomic data were also added that adaptation involved genomic cies electron transfer is often found into the mix. and transcriptomic changes in the in methanogenic environments. The results confirmed that DIET dominant partner, G. sulfurreducens, Although this is mostly thought to was the main mode of electron whereas only transcriptomic changes involve interspecies hydrogen transfer, transfer from G. metallireducens to were observed in G. metallireducens. direct interspecies electron transfer G. sulfurreducens, and showed that This led the authors to suggest that, in (DIET) has been observed in some — in addition to ethanol oxidation syntrophic associations, the electron- methanogenic syntrophies. One and fumarate reduction — nitrogen accepting partner may undergo meta- such laboratory-evolved association fixation by G.
    [Show full text]
  • Syntrophy Between Fermentative and Purple Phototrophic Bacteria For
    bioRxiv preprint doi: https://doi.org/10.1101/2021.05.13.444055; this version posted May 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Original research article 2 3 Syntrophy between fermentative and purple phototrophic bacteria 4 for carbohydrate-based wastewater treatment 5 6 Marta Cerruti1, Guillaume Crosset-Perrotin1, Mythili Ananth1, Jules L. Rombouts1,2 7 and David G. Weissbrodt1,* 8 9 1 Department of Biotechnology, Delft University of Technology, Delft, The Netherlands 10 2 Nature’s Principles B.V., Den Haag, The Netherlands 11 12 * Correspondence: Prof. David Weissbrodt, Weissbrodt Group for Environmental Life Science 13 Engineering, Environmental Biotechnology Section, Department of Biotechnology, TNW Building 14 58, van der Maasweg 9, 2629 HZ Delft, The Netherlands, Tel: +31 15 27 81169; E-mail: 15 [email protected] 16 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.05.13.444055; this version posted May 14, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 17 ABSTRACT 18 Fermentative chemoorganoheterotrophic bacteria (FCB) and purple photoorganoheterotrophic 19 bacteria (PPB) are two interesting microbial guilds to process carbohydrate-rich wastewaters. Their 20 interaction has been studied in axenic pure cultures or co-cultures.
    [Show full text]
  • Microbial Interspecies Interactions: Recent findings in Syntrophic Consortia
    REVIEW published: 13 May 2015 doi: 10.3389/fmicb.2015.00477 Microbial interspecies interactions: recent findings in syntrophic consortia Atsushi Kouzuma1,SouichiroKato2 and Kazuya Watanabe1* 1 School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Tokyo, Japan, 2 Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Sapporo, Japan Microbes are ubiquitous in our biosphere, and inevitably live in communities. They excrete a variety of metabolites and support the growth of other microbes in a community. According to the law of chemical equilibrium, the consumption of excreted metabolites by recipient microbes can accelerate the metabolism of donor microbes. This is the concept of syntrophy, which is a type of mutualism and governs the metabolism and growth of diverse microbes in natural and engineered ecosystems. A representative example of syntrophy is found in methanogenic communities, where Edited by: reducing equivalents, e.g., hydrogen and formate, transfer between syntrophic partners. Amelia-Elena Rotaru, Studies have revealed that microbes involved in syntrophy have evolved molecular University of Southern Denmark, Denmark mechanisms to establish specific partnerships and interspecies communication, Reviewed by: resulting in efficient metabolic cooperation. In addition, recent studies have provided Peter R. Girguis, evidence suggesting that microbial interspecies transfer of reducing equivalents also Harvard University, USA occurs as electric current via biotic (e.g., pili) and abiotic (e.g., conductive mineral Sabine Kleinsteuber, Helmholtz Centre for Environmental and carbon particles) electric conduits. In this review, we describe these findings as Research – UFZ, Germany examples of sophisticated cooperative behavior between different microbial species. *Correspondence: We suggest that these interactions have fundamental roles in shaping the structure and Kazuya Watanabe, School of Life Sciences, Tokyo activity of microbial communities.
    [Show full text]
  • An Oligotrophic Deep-Subsurface Community Dependent on Syntrophy Is Dominated by Sulfur-Driven Autotrophic Denitrifiers
    An oligotrophic deep-subsurface community dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers The MIT Faculty has made this article openly available. Please share how this access benefits you. Your story matters. Citation Lau, Maggie C. Y.; Kieft, Thomas L.; Kuloyo, Olukayode; Linage- Alvarez, Borja; van Heerden, Esta; Lindsay, Melody R.; Magnabosco, Cara, et al. “An Oligotrophic Deep-Subsurface Community Dependent on Syntrophy Is Dominated by Sulfur-Driven Autotrophic Denitrifiers.” Proceedings of the National Academy of Sciences 113, no. 49 (November 2016): E7927–E7936. © 2016 National Academy of Sciences As Published http://dx.doi.org/10.1073/pnas.1612244113 Publisher National Academy of Sciences (U.S.) Version Final published version Citable link http://hdl.handle.net/1721.1/109062 Terms of Use Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. An oligotrophic deep-subsurface community PNAS PLUS dependent on syntrophy is dominated by sulfur-driven autotrophic denitrifiers Maggie C. Y. Laua,1, Thomas L. Kieftb, Olukayode Kuloyoc,2, Borja Linage-Alvarezc,3, Esta van Heerdenc, Melody R. Lindsaya,4, Cara Magnaboscoa,5, Wei Wangd, Jessica B. Wigginsd, Ling Guod, David H. Perlmane,6, Saw Kyine, Henry H. Shwee, Rachel L. Harrisa, Youmi Ohf,7, Min Joo Yig, Roland Purtscherth, Greg F. Slateri, Shuhei Onoj, Siwen Weik, Long Lik,l, Barbara Sherwood Lollarl, and Tullis C. Onstotta aDepartment of Geosciences,
    [Show full text]
  • Inoculum Source Determines Acetate and Lactate Production During Anaerobic Digestion of Sewage Sludge and Food Waste
    bioengineering Article Inoculum Source Determines Acetate and Lactate Production during Anaerobic Digestion of Sewage Sludge and Food Waste Jan Moestedt 1,2, Maria Westerholm 3, Simon Isaksson 3 and Anna Schnürer 1,3,* 1 Department of Thematic Studies–Environmental Change, Linköping University, SE 581 83 Linköping, Sweden; [email protected] 2 Department R&D, Tekniska verken i Linköping AB, SE 581 15 Linköping, Sweden 3 Department of Molecular Sciences, Swedish University of Agricultural Sciences, BioCenter, SE 750 07 Uppsala, Sweden; [email protected] (M.W.); [email protected] (S.I.) * Correspondence: [email protected] Received: 15 November 2019; Accepted: 18 December 2019; Published: 23 December 2019 Abstract: Acetate production from food waste or sewage sludge was evaluated in four semi-continuous anaerobic digestion processes. To examine the importance of inoculum and substrate for acid production, two different inoculum sources (a wastewater treatment plant (WWTP) and a co-digestion plant treating food and industry waste) and two common substrates (sewage sludge and food waste) were used in process operations. The processes were evaluated with regard to the efficiency of hydrolysis, acidogenesis, acetogenesis, and methanogenesis and the microbial community structure was determined. Feeding sewage sludge led to mixed acid fermentation and low total acid yield, whereas feeding food waste resulted in the production of high acetate and lactate yields. Inoculum from WWTP with sewage sludge substrate resulted in maintained methane production, despite a low hydraulic retention time. For food waste, the process using inoculum from WWTP produced high levels of lactate (30 g/L) and acetate (10 g/L), while the process initiated with inoculum from the co-digestion plant had higher acetate (25 g/L) and lower lactate (15 g/L) levels.
    [Show full text]
  • Fermentation of Glucose and Xylose to Hydrogen in the Presence of Long Chain Fatty Acids Stephen Reaume University of Windsor
    View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Scholarship at UWindsor University of Windsor Scholarship at UWindsor Electronic Theses and Dissertations 2009 Fermentation of Glucose and Xylose to Hydrogen in the Presence of Long Chain Fatty Acids Stephen Reaume University of Windsor Follow this and additional works at: http://scholar.uwindsor.ca/etd Recommended Citation Reaume, Stephen, "Fermentation of Glucose and Xylose to Hydrogen in the Presence of Long Chain Fatty Acids" (2009). Electronic Theses and Dissertations. Paper 92. This online database contains the full-text of PhD dissertations and Masters’ theses of University of Windsor students from 1954 forward. These documents are made available for personal study and research purposes only, in accordance with the Canadian Copyright Act and the Creative Commons license—CC BY-NC-ND (Attribution, Non-Commercial, No Derivative Works). Under this license, works must always be attributed to the copyright holder (original author), cannot be used for any commercial purposes, and may not be altered. Any other use would require the permission of the copyright holder. Students may inquire about withdrawing their dissertation and/or thesis from this database. For additional inquiries, please contact the repository administrator via email ([email protected]) or by telephone at 519-253-3000ext. 3208. Fermentation of Glucose and Xylose to Hydrogen in the Presence of Long Chain Fatty Acids by Stephen Reaume A Thesis Submitted to the Faculty of Graduate Studies through the Environmental Engineering Program in Partial Fulfillment of the Requirements for the Degree of Master of Applied Science at the University of Windsor Windsor, Ontario, Canada 2009 © 2009 Stephen Reaume AUTHORS DECLARATION OF ORIGINALITY I hereby certify that I am the sole author of this thesis and that no part of this thesis has been published or submitted for publication.
    [Show full text]
  • Syntrophy Emerges Spontaneously in Complex Metabolic Systems Plos Computational Biology, 15(7): E1007169
    http://www.diva-portal.org This is the published version of a paper published in PloS Computational Biology. Citation for the original published paper (version of record): Libby, E., Hebert-Dufresne, L., Hosseini, S-R., Wagner, A. (2019) Syntrophy emerges spontaneously in complex metabolic systems PloS Computational Biology, 15(7): e1007169 https://doi.org/10.1371/journal.pcbi.1007169 Access to the published version may require subscription. N.B. When citing this work, cite the original published paper. Permanent link to this version: http://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-162885 RESEARCH ARTICLE Syntrophy emerges spontaneously in complex metabolic systems 1,2,3 3,4 5 Eric LibbyID *, Laurent HeÂbert-Dufresne , Sayed-Rzgar HosseiniID , Andreas Wagner3,5 1 Integrated Science Lab, Umeå University, Umeå, Sweden, 2 Department of Mathematics and Mathematical Statistics, Umeå University, Umeå, Sweden, 3 Santa Fe Institute, Santa Fe, New Mexico, United States of America, 4 Department of Computer Science, University of Vermont, Burlington, Vermont, United States of America, 5 Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland a1111111111 a1111111111 * [email protected] a1111111111 a1111111111 a1111111111 Abstract Syntrophy allows a microbial community as a whole to survive in an environment, even though individual microbes cannot. The metabolic interdependence typical of syntrophy is OPEN ACCESS thought to arise from the accumulation of degenerative mutations during the sustained co- evolution of initially self-sufficient organisms. An alternative and underexplored possibility is Citation: Libby E, HeÂbert-Dufresne L, Hosseini S-R, Wagner A (2019) Syntrophy emerges that syntrophy can emerge spontaneously in communities of organisms that did not co- spontaneously in complex metabolic systems.
    [Show full text]
  • Syntrophy in Anaerobic Global Carbon Cycles Michael J Mcinerney1, Jessica R Sieber1 and Robert P Gunsalus2
    Available online at www.sciencedirect.com Syntrophy in anaerobic global carbon cycles Michael J McInerney1, Jessica R Sieber1 and Robert P Gunsalus2 Syntrophy is an essential intermediary step in the anaerobic consumes the product with high affinity (Table 1). For conversion of organic matter to methane where metabolically example, the degradation of butyrate with hydrogen and distinct microorganisms are tightly linked by the need to acetate production is thermodynamically unfavorable maintain the exchanged metabolites at very low unless these metabolites are maintained at very low levels concentrations. Anaerobic syntrophy is thermodynamically by methanogens. This anaerobic metabolism, especially constrained, and is probably a prime reason why it is difficult to when methanogenesis is the driver of the terminal elec- culture microbes as these approaches disrupt consortia. tron accepting reactions, often involves consortia with Reconstruction of artificial syntrophic consortia has allowed tightly coupled syntrophic partnerships [1,2,3]. Syn- uncultured syntrophic metabolizers and methanogens to be trophic interactions also occur in sulfate-reducing optimally grown and studied biochemically. The pathways for environments as evidenced by sulfate-reducing consortia syntrophic acetate, propionate and longer chain fatty acid involved in anaerobic methane oxidation [4]. metabolism are mostly understood, but key steps involved in benzoate breakdown and cyclohexane carboxylate formation Anaerobic syntrophy differs from other types of microbial are unclear. Syntrophic metabolism requires reverse electron metabolism like aerobic fatty acid metabolism or deni- transfer, close physical contact, and metabolic synchronization trification in that a consortium of interacting microbial of the syntrophic partners. Genomic analyses reveal that species rather than a single microbial species is needed to multiple mechanisms exist for reverse electron transfer.
    [Show full text]
  • Potential for Microbial H2 and Metal Transformations Associated with Novel Bacteria and Archaea in Deep Terrestrial Subsurface Sediments
    OPEN The ISME Journal (2017) 11, 1915–1929 www.nature.com/ismej ORIGINAL ARTICLE Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments Alex W Hernsdorf1, Yuki Amano2,3, Kazuya Miyakawa3, Kotaro Ise2, Yohey Suzuki4, Karthik Anantharaman5, Alexander Probst5, David Burstein5, Brian C Thomas5 and Jillian F Banfield5,6 1Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA; 2Nuclear Fuel Cycle Engineering Laboratories, Japan Atomic Energy Agency, Tokai, Ibaraki, Japan; 3Horonobe Underground Research Center, Japan Atomic Energy Agency, Horonobe, Hokkaido, Japan; 4Graduate School of Science, The University of Tokyo, Tokyo, Japan; 5Department of Earth and Planetary Sciences, Berkeley, CA, USA and 6Department of Environmental Science, Policy, and Management, Berkeley, CA, USA Geological sequestration in deep underground repositories is the prevailing proposed route for radioactive waste disposal. After the disposal of radioactive waste in the subsurface, H2 may be produced by corrosion of steel and, ultimately, radionuclides will be exposed to the surrounding environment. To evaluate the potential for microbial activities to impact disposal systems, we explored the microbial community structure and metabolic functions of a sediment-hosted ecosystem at the Horonobe Underground Research Laboratory, Hokkaido, Japan. Overall, we found that the ecosystem hosted organisms from diverse lineages, including many from the phyla that lack isolated representatives. The majority of organisms can metabolize H2, often via oxidative [NiFe] hydrogenases or electron-bifurcating [FeFe] hydrogenases that enable ferredoxin-based pathways, including the ion motive Rnf complex. Many organisms implicated in H2 metabolism are also predicted to catalyze carbon, nitrogen, iron and sulfur transformations.
    [Show full text]