DOCSLIB.ORG

Modulation of Bacterial Multicellularity Via Spatiotemporal Polysaccharide Secretion 2 3 4 Salim T

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Modulation of Bacterial Multicellularity Via Spatiotemporal Polysaccharide Secretion 2 3 4 Salim T bioRxiv preprint doi: https://doi.org/10.1101/2020.02.20.957654; this version posted February 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 Modulation of bacterial multicellularity via spatiotemporal polysaccharide secretion 2 3 4 Salim T. Islam1,2,3†*, Israel Vergara Alvarez3†, Fares Saïdi1,2,3†, Annick Giuseppi3, Evgeny 5 Vinogradov4, Castrese Morrone3, Gael Brasseur3, Gaurav Sharma5,6, Anaïs Benarouche7, Jean- 6 Luc Bridot7, Gokulakrishnan Ravicoularamin1, Alain Cagna7, Charles Gauthier1, Mitchell 7 Singer5, Henri-Pierre Fierobe3, Tâm Mignot3, Emilia M. F. Mauriello3* 8 9 1 Armand Frappier Health & Biotechnology Research Centre, Institut National de la Recherche 10 Scientifique, Université du Québec, Institut Pasteur International Network, Laval, QC, Canada 11 2 PROTEO, the Quebec Network for Research on Protein Function, Engineering, and 12 Applications, Université Laval, Quebec, QC, Canada 13 3 Laboratoire de Chimie Bactérienne, CNRS - Université Aix-Marseille UMR7283, Institut de 14 Microbiologie de la Méditerranée, Marseille, France 15 4 National Research Council, 100 Sussex Dr., Ottawa, Ontario, Canada 16 5 Department of Microbiology and Molecular Genetics, University of California – Davis, Davis, 17 CA, USA 18 6 Institute of Bioinformatics and Applied Biotechnology, Electronic City, Bengaluru, Karnataka, 19 560100, India 20 7 Teclis Scientific, Civrieux d’Azergue, France 21 22 †equal contribution 23 24 25 *co-corresponding authors 26 27 Salim T. Islam Emilia M. F. Mauriello 28 E-mail: [email protected] E-mail: [email protected] 29 Phone: (+1) 450-687-5010 ext. 8897 Phone: (+33) 04 91 16 43 21 Page 1 of 52 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.20.957654; this version posted February 20, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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. 30 ABSTRACT: 31 The development of multicellularity is a key evolutionary transition allowing for 32 differentiation of physiological functions across a cell population that confers survival benefits; 33 among unicellular bacteria, this can lead to complex developmental behaviours and the 34 formation of higher-order community structures. Herein, we demonstrate that in the social δ- 35 proteobacterium Myxococcus xanthus, the secretion of a novel secreted biosurfactant 36 polysaccharide (BPS) is temporally and spatially modulated within communities, mediating 37 swarm migration as well as the formation of multicellular swarm biofilms and fruiting bodies. 38 BPS is a type IV pilus-inhibited acidic polymer built of randomly-acetylated β-linked 39 tetrasaccharide repeats. Both BPS and the “shared good” EPS are produced by dedicated 40 Wzx/Wzy-dependent polysaccharide assembly pathways distinct from that responsible for spore 41 coat assembly. To our knowledge, such pathways have never-before been explicitly shown to 42 synthesize a biosurfactant. Together, these data reveal the central role of secreted 43 polysaccharides in the intricate behaviours coordinating bacterial multicellularity. Page 2 of 52 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.20.957654; this version posted February 20, 2020. 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. 44 INTRODUCTION: 45 Multicellularity is denoted by the differentiation of physiological functions across a 46 contiguous cell population, with its development regarded as a key evolutionary transition [1]. 47 To attain this level of organizational complexity, cells generally must be able to proliferate, 48 specialize, communicate, interact, and move, with these behaviours promoting an increase in the 49 size of a cell collective and the development of higher-order structures [2]. Though typically 50 associated with metazoan organisms, multicellular physiology is also displayed by bacteria, with 51 the best-studied examples being the formation of biofilms and fruiting bodies [3-6]. 52 Secreted long-chain polysaccharides are an important mediator of multicellularity as they 53 serve to retain and organize cells as well as to physically and biochemically buffer the 54 community within the context of an extracellular matrix [7], thus enhancing survival and fitness. 55 Monospecies bacterial biofilms have thus been intensively studied with respect to their effects on 56 inter-cell communication, leading to differences in gene regulation and changes in matrix 57 polysaccharide production. However, in-depth knowledge of the mechanisms used by bacteria to 58 modulate multicellular physiology in such communities is limited. 59 Due to its complex social predatory lifecycle, the Gram-negative δ-proteobacterium 60 Myxococcus xanthus has emerged as a leading model system in which to simultaneously study 61 multiple factors contributing to organizational complexity. This soil bacterium is capable of 62 saprophytic feeding on products derived from predation of other bacteria [8]. Two forms of 63 motility are required for this complex physiology: type IV pilus (T4P)-dependent group (i.e. 64 “social” [S]) motility [9, 10] on soft surfaces, and single-cell gliding (i.e. “adventurous” [A]) 65 motility on hard surfaces mediated by directed transport and substratum coupling of the Agl–Glt 66 trans-envelope complex [11, 12]. Upon local nutrient depletion, cells initiate a developmental Page 3 of 52 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.20.957654; this version posted February 20, 2020. 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. 67 cycle resulting in aggregation and fruiting body formation within 72 h, generating three 68 differentiated cell subpopulations: (i) cells that form desiccation-resistant myxospores in the 69 centre of the fruiting body, (ii) those that remain at the base of the fruiting body, termed 70 “peripheral rods”, and (iii) forager cells that continue their outward motility away from the 71 fruiting body [13]. 72 M. xanthus produces several known long-chain polysaccharides that are central to its 73 complex lifecycle. In addition to the O-antigen polymer that caps its LPS and is implicated in 74 motility [14-16], M. xanthus biosynthesizes a poorly characterized “slime” polysaccharide that 75 facilitates adhesion of the Glt gliding motility complex proteins to the substratum, and is 76 deposited in trails behind surface-gliding cells [17, 18]. Exopolysaccharide (EPS) is a specific 77 secreted polymer of this bacterium that is important for T4P-dependent swarm spreading; it is 78 also crucial for biofilm formation as it constitutes a large portion of the extracellular matrix in 79 stationary M. xanthus biofilms and connects cells via a network of fibrils [19-21]. The 80 production of EPS requires the presence of a T4P [22], which affects the Dif chemosensory 81 pathway (reviewed elsewhere [13]). Finally, cells undergoing sporulation synthesize the major 82 spore coat (MASC) polymer that surrounds myxospores [23, 24]. 83 The most widespread polysaccharide biosynthesis paradigm is the flippase/polymerase 84 (Wzx/Wzy)-dependent pathway [25]. It is used by Gram-negative and Gram-positive bacteria as 85 well as Archaea to produce a wide range of secreted and/or cell surface-associated bacterial 86 polymers [26] including capsular polysaccharide, adhesive hold-fast polymer, spore-coat 87 polymer, O-antigen, and exopolysaccharide [27, 28]. Wzx/Wzy-dependent polysaccharide 88 assembly is a complex process [29] involving a suite of integral inner-membrane (IM) proteins 89 containing multiple α-helical transmembrane segments (TMS) [30]. At the cytoplasmic leaflet of Page 4 of 52 bioRxiv preprint doi: https://doi.org/10.1101/2020.02.20.957654; this version posted February 20, 2020. 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. 90 the IM, individual polysaccharide repeat units are built on an undecaprenyl pyrophosphate 91 (UndPP) carrier. UndPP-linked repeats are then translocated across the IM by the Wzx flippase 92 [31, 32] via a putative antiport mechanism [33, 34]. Defects in this step, resulting in a buildup of 93 UndPP-linked repeat units for a given pathway, can have adverse effects on cell growth as well 94 as polysaccharide synthesis by other pathways in the same cell, all dependent on UndPP-linked 95 sugars [35]. Once in the periplasmic leaflet of the IM, repeat units are joined together by two 96 key periplasmic loops of the Wzy polymerase [36-39], resulting in polymer extension at the 97 reducing terminus of the growing chain [40]. Repeat-polymerization defects in a given pathway 98 requiring UndPP may also affect other pathways requiring UndPP due to sequestration of the 99 cellular UndPP pool. Associated polysaccharide co-polymerase
Load more

Recommended publications
  • CUED Phd and Mphil Thesis Classes
    High-throughput Experimental and Computational Studies of Bacterial Evolution Lars Barquist Queens' College University of Cambridge A thesis submitted for the degree of Doctor of Philosophy 23 August 2013 Arrakis teaches the attitude of the knife { chopping off what's incomplete and saying: \Now it's complete because it's ended here." Collected Sayings of Muad'dib Declaration High-throughput Experimental and Computational Studies of Bacterial Evolution The work presented in this dissertation was carried out at the Wellcome Trust Sanger Institute between October 2009 and August 2013. This dissertation is the result of my own work and includes nothing which is the outcome of work done in collaboration except where specifically indicated in the text. This dissertation does not exceed the limit of 60,000 words as specified by the Faculty of Biology Degree Committee. This dissertation has been typeset in 12pt Computer Modern font using LATEX according to the specifications set by the Board of Graduate Studies and the Faculty of Biology Degree Committee. No part of this dissertation or anything substantially similar has been or is being submitted for any other qualification at any other university. Acknowledgements I have been tremendously fortunate to spend the past four years on the Wellcome Trust Genome Campus at the Sanger Institute and the European Bioinformatics Institute. I would like to thank foremost my main collaborators on the studies described in this thesis: Paul Gardner and Gemma Langridge. Their contributions and support have been invaluable. I would also like to thank my supervisor, Alex Bateman, for giving me the freedom to pursue a wide range of projects during my time in his group and for advice.
    [Show full text]
  • Thèse Morgane Wartel
    Faculté des Sciences - Aix-Marseille Université Laboratoire de Chimie Bactérienne 163 Avenue de Luminy - Case 901 31 Chemin Joseph Aiguier 13288 Marseille 13009 Marseille Thèse En vue d’obtenir le grade de Docteur d’Aix-Marseille Université Biologie, spécialité Microbiologie Présentée et soutenue publiquement par Morgane Wartel Le Mercredi 18 Décembre 2013 A novel class of bacterial motors involved in the directional transport of a sugar at the bacterial surface: The machineries of motility and sporulation in Myxococcus xanthus. Une nouvelle classe de moteurs bactériens impliqués dans le transport de macromolécules à la surface bactérienne: Les machineries de motilité et de sporulation de Myxococcus xanthus. Membres du Jury : Dr. Christophe Grangeasse Rapporteur Dr. Patrick Viollier Rapporteur Pr. Pascale Cossart Examinateur Dr. Francis-André Wollman Examinateur Dr. Tâm Mignot Directeur de Thèse Pr. Frédéric Barras Président du Jury Faculté des Sciences - Aix-Marseille Université Laboratoire de Chimie Bactérienne 163 Avenue de Luminy - Case 901 31 Chemin Joseph Aiguier 13288 Marseille 13009 Marseille Thèse En vue d’obtenir le grade de Docteur d’Aix-Marseille Université Biologie, spécialité Microbiologie Présentée et soutenue publiquement par Morgane Wartel Le Mercredi 18 Décembre 2013 A novel class of bacterial motors involved in the directional transport of a sugar at the bacterial surface: The machineries of motility and sporulation in Myxococcus xanthus. Une nouvelle classe de moteurs bactériens impliqués dans le transport de macromolécules à la surface bactérienne: Les machineries de motilité et de sporulation de Myxococcus xanthus. Membres du Jury : Dr. Christophe Grangeasse Rapporteur Dr. Patrick Viollier Rapporteur Pr. Pascale Cossart Examinateur Dr. Francis-André Wollman Examinateur Dr.
    [Show full text]
  • J. Gen. Appl. Microbiol., 48, 109–115 (2002)
    J. Gen. Appl. Microbiol., 48, 109–115 (2002) Full Paper Haliangium ochraceum gen. nov., sp. nov. and Haliangium tepidum sp. nov.: Novel moderately halophilic myxobacteria isolated from coastal saline environments Ryosuke Fudou,* Yasuko Jojima, Takashi Iizuka, and Shigeru Yamanaka† Central Research Laboratories, Ajinomoto Co., Inc., Kawasaki 210–8681, Japan (Received November 21, 2001; Accepted January 31, 2002) Phenotypic and phylogenetic studies were performed on two myxobacterial strains, SMP-2 and SMP-10, isolated from coastal regions. The two strains are morphologically similar, in that both produce yellow fruiting bodies, comprising several sessile sporangioles in dense packs. They are differentiated from known terrestrial myxobacteria on the basis of salt requirements (2–3% NaCl) and the presence of anteiso-branched fatty acids. Comparative 16S rRNA gene sequencing studies revealed that SMP-2 and SMP-10 are genetically related, and constitute a new cluster within the myxobacteria group, together with the Polyangium vitellinum Pl vt1 strain as the clos- est neighbor. The sequence similarity between the two strains is 95.6%. Based on phenotypic and phylogenetic evidence, it is proposed that these two strains be assigned to a new genus, JCM؍) .Haliangium gen. nov., with SMP-2 designated as Haliangium ochraceum sp. nov .(DSM 14436T؍JCM 11304T؍) .DSM 14365T), and SMP-10 as Haliangium tepidum sp. nov؍11303T Key Words——Haliangium gen. nov.; Haliangium ochraceum sp. nov.; Haliangium tepidum sp. nov.; marine myxobacteria Introduction terized as Gram-negative, rod-shaped gliding bacteria with high GϩC content. Analyses of 16S rRNA gene Myxobacteria are unique in their complex life cycle. sequences reveal that they form a relatively homoge- Under starvation conditions, bacterial cells gather to- neous cluster within the d-subclass of Proteobacteria gether to form aggregates that subsequently differenti- (Shimkets and Woese, 1992).
    [Show full text]
  • Marine Myxobacteria As a Source of Antibiotics—Comparison of Physiology, Polyketide-Type Genes and Antibiotic Production of Three New Isolates of Enhygromyxa Salina
    View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by PubMed Central Mar. Drugs 2010, 8, 2466-2479; doi:10.3390/md8092466 OPEN ACCESS Marine Drugs ISSN 1660-3397 www.mdpi.com/journal/marinedrugs Article Marine Myxobacteria as a Source of Antibiotics—Comparison of Physiology, Polyketide-Type Genes and Antibiotic Production of Three New Isolates of Enhygromyxa salina Till F. Schäberle 1, Emilie Goralski 1, Edith Neu 1, Özlem Erol 1, Georg Hölzl 2, Peter Dörmann 2, Gabriele Bierbaum 3 and Gabriele M. König 1,* 1 Institute of Pharmaceutical Biology, University of Bonn, Nussallee 6, 53115 Bonn, Germany; E-Mails: [email protected] (T.F.S.); [email protected] (E.G.); [email protected] (E.N.); [email protected] (Ö.E.) 2 Institute of Molecular Physiology and Biotechnology of Plants (IMBIO), University of Bonn, Karlrobert-Kreiten-Str. 13, 53115 Bonn, Germany; E-Mails: [email protected] (G.H.); [email protected] (P.D.) 3 Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University of Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany; E-Mail: [email protected] (G.B.) * Author to whom correspondence should be addressed; E-Mail: [email protected]; Tel.: +49-228-733747; Fax: +49-228-733250. Received: 12 August 2010; in revised form: 25 August 2010 / Accepted: 1 September 2010 / Published: 3 September 2010 Abstract: Three myxobacterial strains, designated SWB004, SWB005 and SWB006, were obtained from beach sand samples from the Pacific Ocean and the North Sea.
    [Show full text]
  • Mining the Yucatan Coastal Microbiome for the Identification of Non
    toxins Article Mining the Yucatan Coastal Microbiome for the Identification of Non-Ribosomal Peptides Synthetase (NRPS) Genes Mario Alberto Martínez-Núñez * and Zuemy Rodríguez-Escamilla * UMDI-Sisal, Facultad de Ciencias, Universidad Nacional Autónoma de México, Puerto de Abrigo s/n, Sisal, Yucatán CP 97355, Mexico * Correspondence: [email protected] (M.A.M.-N.); [email protected] (Z.R.-E.); Tel.: +52-999-341-0860 (ext. 7631) (M.A.M.-N.) Received: 21 February 2020; Accepted: 16 April 2020; Published: 26 May 2020 Abstract: Prokaryotes represent a source of both biotechnological and pharmaceutical molecules of importance, such as nonribosomal peptides (NRPs). NRPs are secondary metabolites which their synthesis is independent of ribosomes. Traditionally, obtaining NRPs had focused on organisms from terrestrial environments, but in recent years marine and coastal environments have emerged as an important source for the search and obtaining of nonribosomal compounds. In this study, we carried out a metataxonomic analysis of sediment of the coast of Yucatan in order to evaluate the potential of the microbial communities to contain bacteria involved in the synthesis of NRPs in two sites: one contaminated and the other conserved. As well as a metatranscriptomic analysis to discover nonribosomal peptide synthetases (NRPSs) genes. We found that the phyla with the highest representation of NRPs producing organisms were the Proteobacteria and Firmicutes present in the sediments of the conserved site. Similarly, the metatranscriptomic analysis showed that 52% of the sequences identified as catalytic domains of NRPSs were found in the conserved site sample, mostly (82%) belonging to Proteobacteria and Firmicutes; while the representation of Actinobacteria traditionally described as the major producers of secondary metabolites was low.
    [Show full text]
  • Marine-Derived Myxobacteria of the Suborder Nannocystineae: an Underexplored Source of Structurally Intriguing and Biologically Active Metabolites
    Marine-derived myxobacteria of the suborder Nannocystineae: An underexplored source of structurally intriguing and biologically active metabolites Antonio Dávila-Céspedes‡, Peter Hufendiek‡, Max Crüsemann‡, Till F. Schäberle and Gabriele M. König* Review Open Access Address: Beilstein J. Org. Chem. 2016, 12, 969–984. Institute for Pharmaceutical Biology, University of Bonn, Nussallee 6, doi:10.3762/bjoc.12.96 53115 Bonn, Germany Received: 22 February 2016 Email: Accepted: 25 April 2016 Gabriele M. König* - [email protected] Published: 13 May 2016 * Corresponding author ‡ Equal contributors This article is part of the Thematic Series "Natural products in synthesis and biosynthesis II". Keywords: Enhygromyxa; genome mining; myxobacteria; Nannocystineae; Guest Editor: J. S. Dickschat natural products © 2016 Dávila-Céspedes et al; licensee Beilstein-Institut. License and terms: see end of document. Abstract Myxobacteria are famous for their ability to produce most intriguing secondary metabolites. Till recently, only terrestrial myxobac- teria were in the focus of research. In this review, however, we discuss marine-derived myxobacteria, which are particularly inter- esting due to their relatively recent discovery and due to the fact that their very existence was called into question. The to-date- explored members of these halophilic or halotolerant myxobacteria are all grouped into the suborder Nannocystineae. Few of them were chemically investigated revealing around 11 structural types belonging to the polyketide, non-ribosomal peptide, hybrids thereof or terpenoid class of secondary metabolites. A most unusual structural type is represented by salimabromide from Enhygromyxa salina. In silico analyses were carried out on the available genome sequences of four bacterial members of the Nannocystineae, revealing the biosynthetic potential of these bacteria.
    [Show full text]
  • The Soil Microbial Food Web Revisited: Predatory Myxobacteria As Keystone Taxa?
    The ISME Journal https://doi.org/10.1038/s41396-021-00958-2 ARTICLE The soil microbial food web revisited: Predatory myxobacteria as keystone taxa? 1 1 1,2 1 1 Sebastian Petters ● Verena Groß ● Andrea Söllinger ● Michelle Pichler ● Anne Reinhard ● 1 1 Mia Maria Bengtsson ● Tim Urich Received: 4 October 2018 / Revised: 24 February 2021 / Accepted: 4 March 2021 © The Author(s) 2021. This article is published with open access Abstract Trophic interactions are crucial for carbon cycling in food webs. Traditionally, eukaryotic micropredators are considered the major micropredators of bacteria in soils, although bacteria like myxobacteria and Bdellovibrio are also known bacterivores. Until recently, it was impossible to assess the abundance of prokaryotes and eukaryotes in soil food webs simultaneously. Using metatranscriptomic three-domain community profiling we identified pro- and eukaryotic micropredators in 11 European mineral and organic soils from different climes. Myxobacteria comprised 1.5–9.7% of all obtained SSU rRNA transcripts and more than 60% of all identified potential bacterivores in most soils. The name-giving and well-characterized fi 1234567890();,: 1234567890();,: predatory bacteria af liated with the Myxococcaceae were barely present, while Haliangiaceae and Polyangiaceae dominated. In predation assays, representatives of the latter showed prey spectra as broad as the Myxococcaceae. 18S rRNA transcripts from eukaryotic micropredators, like amoeba and nematodes, were generally less abundant than myxobacterial 16S rRNA transcripts, especially in mineral soils. Although SSU rRNA does not directly reflect organismic abundance, our findings indicate that myxobacteria could be keystone taxa in the soil microbial food web, with potential impact on prokaryotic community composition.
    [Show full text]
  • Bacterial Microcompartments
    HHS Public Access Author manuscript Author ManuscriptAuthor Manuscript Author Nat Rev Manuscript Author Microbiol. Author Manuscript Author manuscript; available in PMC 2018 November 01. Published in final edited form as: Nat Rev Microbiol. 2018 May ; 16(5): 277–290. doi:10.1038/nrmicro.2018.10. Bacterial microcompartments Cheryl A. Kerfeld1,2,3,*, Clement Aussignargues1,3, Jan Zarzycki4, Fei Cai2, and Markus Sutter1,2,3 1MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI 48824, USA 2Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA 3Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824, USA 4Max-Planck-Institute for Terrestrial Microbiology, D-35043, Marburg, Germany Abstract Bacterial microcompartments (BMCs) are self-assembling organelles that consist of an enzymatic core that is encapsulated by a selectively permeable protein shell. The potential to form BMCs is widespread, found across the Kingdom Bacteria. BMCs have crucial roles in carbon dioxide fixation in autotrophs and the catabolism of organic substrates in heterotrophs. They contribute to the metabolic versatility of bacteria, providing a competitive advantage in specific environmental niches. Although BMCs were first visualized more than sixty years ago, it is mainly in the last decade that progress has been made in understanding their metabolic diversity and the structural basis of their assembly and function. This progress has not only heightened our understanding of their role in microbial metabolism but it is also beginning to enable their use in a variety of applications in synthetic biology. In this Review, we focus on recent insights into the structure, assembly, diversity and function of BMCs.
    [Show full text]
  • Phylogenetic Profile of Copper Homeostasis in Deltaproteobacteria
    Phylogenetic Profile of Copper Homeostasis in Deltaproteobacteria A Major Qualifying Report Submitted to the Faculty of Worcester Polytechnic Institute In Partial Fulfillment of the Requirements for the Degree of Bachelor of Science By: __________________________ Courtney McCann Date Approved: _______________________ Professor José M. Argüello Biochemistry WPI Project Advisor 1 Abstract Copper homeostasis is achieved in bacteria through a combination of copper chaperones and transporting and chelating proteins. Bioinformatic analyses were used to identify which of these proteins are present in Deltaproteobacteria. The genetic environment of the bacteria is affected by its lifestyle, as those that live in higher concentrations of copper have more of these proteins. Two major transport proteins, CopA and CusC, were found to cluster together frequently in the genomes and appear integral to copper homeostasis in Deltaproteobacteria. 2 Acknowledgements I would like to thank Professor José Argüello for giving me the opportunity to work in his lab and do some incredible research with some equally incredible scientists. I need to give all of my thanks to my supervisor, Dr. Teresita Padilla-Benavides, for having me as her student and teaching me not only lab techniques, but also how to be scientist. I would also like to thank Dr. Georgina Hernández-Montes and Dr. Brenda Valderrama from the Insituto de Biotecnología at Universidad Nacional Autónoma de México (IBT-UNAM), Campus Morelos for hosting me and giving me the opportunity to work in their lab. I would like to thank Sarju Patel, Evren Kocabas, and Jessica Collins, whom I’ve worked alongside in the lab. I owe so much to these people, and their support and guidance has and will be invaluable to me as I move forward in my education and career.
    [Show full text]
  • Isolation and Biosynthetic Analysis of Haliamide, a New PKS-NRPS Hybrid Metabolite from the Marine Myxobacterium Haliangium Ochraceum
    molecules Article Isolation and Biosynthetic Analysis of Haliamide, a New PKS-NRPS Hybrid Metabolite from the Marine Myxobacterium Haliangium ochraceum Yuwei Sun 1, Tomohiko Tomura 1, Junichi Sato 1, Takashi Iizuka 2, Ryosuke Fudou 3 and Makoto Ojika 1,* Received: 11 November 2015 ; Accepted: 31 December 2015 ; Published: 6 January 2016 Academic Editor: Derek J. McPhee 1 Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan; [email protected] (Y.S.); [email protected] (T.T.); [email protected] (J.S.) 2 Institute for Innovation, Ajinomoto Co., Inc., Kawasaki, Kanagawa 210-8681, Japan; [email protected] 3 R & D Planning Department, Ajinomoto Co., Inc., Chuo-ku, Tokyo 104-8315, Japan; [email protected] * Correspondence: [email protected]; Tel.: +81-52-789-4116; Fax: +81-52-789-4118 Abstract: Myxobacteria of marine origin are rare and hard-to-culture microorganisms, but they genetically harbor high potential to produce novel antibiotics. An extensive investigation on the secondary metabolome of the unique marine myxobacterium Haliangium ochraceum SMP-2 led to the isolation of a new polyketide-nonribosomal peptide hybrid product, haliamide (1). Its structure was elucidated by spectroscopic analyses including NMR and HR-MS. Haliamide (1) showed cytotoxicity against HeLa-S3 cells with IC50 of 12 µM. Feeding experiments were performed to identify the biosynthetic building blocks of 1, revealing one benzoate, one alanine, two propionates, one acetate and one acetate-derived terminal methylene. The biosynthetic gene cluster of haliamide (hla, 21.7 kbp) was characterized through the genome mining of the producer, allowing us to establish a model for the haliamide biosynthesis.
    [Show full text]
  • A Recent Evolutionary Origin of a Bacterial Small RNA That Controls
    Molecular Phylogenetics and Evolution 73 (2014) 1–9 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev A recent evolutionary origin of a bacterial small RNA that controls multicellular fruiting body development q ⇑ I-Chen Kimberly Chen a,b, , Brad Griesenauer a, Yuen-Tsu Nicco Yu b, Gregory J. Velicer a,b a Department of Biology, Indiana University, Bloomington, IN 47405, USA b Institute of Integrative Biology (IBZ), ETH Zurich, CH-8092 Zurich, Switzerland article info abstract Article history: In animals and plants, non-coding small RNAs regulate the expression of many genes at the post-tran- Received 26 August 2013 scriptional level. Recently, many non-coding small RNAs (sRNAs) have also been found to regulate a vari- Revised 30 December 2013 ety of important biological processes in bacteria, including social traits, but little is known about the Accepted 2 January 2014 phylogenetic or mechanistic origins of such bacterial sRNAs. Here we propose a phylogenetic origin of Available online 10 January 2014 the myxobacterial sRNA Pxr, which negatively regulates the initiation of fruiting body development in Myxococcus xanthus as a function of nutrient level, and also examine its diversification within the Keywords: Myxococcocales order. Homologs of pxr were found throughout the Cystobacterineae suborder (with a Bacterial development few possible losses) but not outside this clade, suggesting a single origin of the Pxr regulatory system Multicellularity Myxobacteria in the basal Cystobacterineae lineage. Rates of pxr sequence evolution varied greatly across Cystobacte- Non-coding small RNAs rineae sub-clades in a manner not predicted by overall genome divergence.
    [Show full text]
  • Maxbin: an Automated Binning Method to Recover Individual
    Wu et al. Microbiome 2014, 2:26 http://www.microbiomejournal.com/content/2/1/26 METHODOLOGY Open Access MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm Yu-Wei Wu1,2*, Yung-Hsu Tang1,3, Susannah G Tringe4,5, Blake A Simmons1,6 and Steven W Singer1,7 Abstract Background: Recovering individual genomes from metagenomic datasets allows access to uncultivated microbial populations that may have important roles in natural and engineered ecosystems. Understanding the roles of these uncultivated populations has broad application in ecology, evolution, biotechnology and medicine. Accurate binning of assembled metagenomic sequences is an essential step in recovering the genomes and understanding microbial functions. Results: We have developed a binning algorithm, MaxBin, which automates the binning of assembled metagenomic scaffolds using an expectation-maximization algorithm after the assembly of metagenomic sequencing reads. Binning of simulated metagenomic datasets demonstrated that MaxBin had high levels of accuracy in binning microbial genomes. MaxBin was used to recover genomes from metagenomic data obtained through the Human Microbiome Project, which demonstrated its ability to recover genomes from real metagenomic datasets with variable sequencing coverages. Application of MaxBin to metagenomes obtained from microbial consortia adapted to grow on cellulose allowed genomic analysis of new, uncultivated, cellulolytic bacterial populations, including an abundant myxobacterial population distantly related to Sorangium cellulosum that possessed a much smaller genome (5 MB versus 13 to 14 MB) but has a more extensive set of genes for biomass deconstruction. For the cellulolytic consortia, the MaxBin results were compared to binning using emergent self-organizing maps (ESOMs) and differential coverage binning, demonstrating that it performed comparably to these methods but had distinct advantages in automation, resolution of related genomes and sensitivity.
    [Show full text]