BERGEY’S MANUAL® OF Systematic Bacteriology Second Edition

Volume Five The , Part A and B BERGEY’S MANUAL® OF Systematic Bacteriology Second Edition

Volume Five The Actinobacteria, Part A and B

Michael Goodfellow, Peter Kämpfer, Hans-Jürgen Busse, Martha E. Trujillo, Ken-ichiro Suzuki, Wolfgang Ludwig and William B. Whitman EDITORS, VOLUME FIVE William B. Whitman DIRECTOR OF THE EDITORIAL OFFICE Aidan C. Parte MANAGING EDITOR

EDITORIAL BOARD Fred A. Rainey, Chairman, Peter Kämpfer, Vice Chairman, Paul De Vos, Jongsik Chun, Martha E. Trujillo and William B. Whitman WITH CONTRIBUTIONS FROM 116 COLLEAGUES William B. Whitman Bergey’s Manual Trust Department of Microbiology 527 Biological Sciences Building University of Georgia Athens, GA 30602-2605 USA

ISBN 978-0-387-95043-3 ISBN 978-0-387-68233-4 (eBook) DOI 10.1007/978-0-387-68233-4 Springer New York Dordrecht Heidelberg London

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© 2012, 1984–1989 Bergey’s Manual Trust

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Springer is part of Springer Science+Business Media (www.springer.com) This volume is dedicated to our colleagues Michael Goodfellow and Peter H.A. Sneath.

Michael retired from the Board of Trustees of Bergey’s Manual during preparation of this volume. His tremendous efforts as an editor, author and officer of the Trust are truly appreciated.

Our late eminent colleague Peter H.A. Sneath (1923–2011) was a Trustee (1978–1994) and Chairman of the Trust (1990–1994). He also served as an editor of previous editions of The Manual and made many other remarkable contributions to the systematics of . EDITORIAL BOARD AND TRUSTEES OF BERGEY’S MANUAL TRUST

Fred A. Rainey, Chairman Peter Kämpfer, Vice Chairman Jongsik Chun Paul De Vos Martha E. Trujillo William B. Whitman

Don J. Brenner, Emeritus Richard W. Castenholz, Emeritus George M. Garrity, Emeritus Michael Goodfellow, Emeritus John G. Holt, Emeritus Noel R. Krieg, Emeritus John Liston, Emeritus James W. Moulder, Emeritus R.G.E. Murray, Emeritus Karl-Heinz Schleifer, Emeritus James T. Staley, Emeritus Joseph G. Tully, Emeritus Preface to volume 5 of the second edition of Bergey’s Manual ® of Systematic Bacteriology

Prokaryotic systematics remains a vibrant and exciting field The Trust recognizes its enormous debt to Dr Aidan Parte, of study, one of challenges and opportunities, great discover- whose enthusiasm and professionalism have made this Manual ies and gradual advances. To honor one of the leaders of our possible. The completion of the second edition is due in great field, the Trust presented the Bergey Award in recognition of measure to his dedication, good judgment, and hard work. His outstanding contributions to the of prokaryotes to vision for excellent science has made the Manual more than it Antonio Ventosa in 2010. The Bergey Medal, in recognition of would have been. life-long contributions to the field of systematic bacteriology, We also recognize the special efforts of Dr Jean Euzéby in was also awarded to Michael Goodfellow, Zhiheng Liu, Ji-Sheng checking and correcting where necessary the nomenclature Ruan, and James Tiedje in 2011. and etymology of every described taxon in this volume. Volume 5 will be the last volume to be edited by Michael Good- The Trust also thanks its Springer colleagues, especially fellow, who served on the Trust for many years and has continued Editorial Director Andrea Macaluso and Production Manager to be active during his retirement. Mike contributed to volumes 2 Susan Westendorf, for all of their efforts. As this will be the last and 4 of the first edition of Bergey’s Manual of Systematic Bacteriology volume of the Manual published in collaboration with Springer, and has made an enormous contribution to the present volume the Trust also wishes to acknowledge the tremendous support as an author, editor, and mentor. As a leader in actinobacterial and understanding that Springer has demonstrated over the research for many decades, he is also directly responsible for last 13 years in helping us to publish this comprehensive synthesis much of the wealth of information about this fascinating group of of the systematics of prokaryotes. microorganisms described in the current volume. Mike served as In addition, we thank Amina Ravi, our manager at our type- the Vice-Chairman of the Trust for many years and Chairman for setters, SPi, for her work in the proofing and production of this the last 3 years. During his tenure, the Trust underwent impor- and the previous two volumes. tant transitions for the future beyond the second edition. Adept We thank our current copyeditors, proofreaders and other at saying the most difficult things in the nicest way and a master of staff, including Susan Andrews, Joanne Auger, Hannah Berle, the telling omission, he was the right person at the right time. Robert Gutman, Judy Leventhal, Linda Sanders, Tyler Sgro, Dana Schneider, and Mohammed Waqar, without whose hard Acknowledgements work and attention to detail the production of this volume The Trust is indebted to all of the contributors and reviewers, would have been impossible. Lastly, we thank Dale Boyer and without whom this work would not be possible. The Editors the other members of the Department of Microbiology at are grateful for the time and effort that each has expended on the University of Georgia for their unfailing support of this behalf of the entire scientific community. We also thank the endeavor. authors for their good grace in accepting comments, criticisms, and editing of their manuscripts. William B. (Barny) Whitman

ix Contents

Preface to volume 5 ...... ix Contributors ...... xvii On using the Manual ...... xxiii Part A Road map of the phylum Actinobacteria ...... 1 Taxonomic outline of the phylum Actinobacteria ...... 29 Phylum XXVI. Actinobacteria phyl. nov...... 33 Class I. Actinobacteria ...... 34 Order I. ...... 35 Family I. Actinomycetaceae ...... 36 Genus I. Actinomyces ...... 42 Genus II. Actinobaculum ...... 109 Genus III. ...... 114 Genus IV. Mobiluncus ...... 126 Genus V. Varibaculum ...... 139 Order II. Actinopolysporales ord. nov...... 162 Family I. Actinopolysporaceae ...... 163 Genus I. Actinopolyspora ...... 163 Order III. Bifidobacteriales ...... 170 Family I. Bifidobacteriaceae ...... 171 Genus I. Bifidobacterium ...... 171 Genus II. Aeriscardovia ...... 206 Genus III. Alloscardovia ...... 207 Genus IV. Gardnerella ...... 208 Genus V. Metascardovia ...... 211 Genus VI. Parascardovia ...... 213 Genus VII. Scardovia ...... 214 Order IV. ord. nov...... 225 Family I. Catenulisporaceae ...... 226 Genus I. ...... 226 Family II. ...... 232 Genus I. ...... 232 Order V. Corynebacteriales ord. nov...... 235 Family I. Corynebacteriaceae ...... 244 Genus I. ...... 245 Genus II. Turicella ...... 289 Family II. Dietziaceae ...... 301 Genus I. Dietzia ...... 301 Family III. Mycobacteriaceae ...... 312 Genus I. ...... 312

xi xii CONTENTS

Family IV. Nocardiaceae ...... 376 Genus I. ...... 376 Genus II. Gordonia ...... 419 Genus III. Millisia ...... 435 Genus IV. ...... 437 Genus V. Skermania ...... 464 Genus VI. Smaragdicoccus ...... 467 Genus VII. Williamsia ...... 470 Family V. Segniliparaceae ...... 497 Genus I. Segniliparus ...... 497 Family VI. Tsukamurellaceae ...... 500 Genus I. Tsukamurella ...... 500 Order VI. Frankiales ord. nov ...... 509 Family I. Frankiaceae ...... 512 Genus I. Frankia ...... 512 Family II. Acidothermaceae ...... 520 Genus I. Acidothermus ...... 520 Family III. ...... 522 Genus I. Cryptosporangium ...... 522 Genus Incertae sedis I. Fodinicola ...... 525 Family IV. Geodermatophilaceae ...... 528 Genus I. Geodermatophilus ...... 528 Genus II. Blastococcus ...... 531 Genus III. Modestobacter ...... 536 Family V. Nakamurellaceae ...... 539 Genus I. Nakamurella ...... 540 Genus II. Humicoccus ...... 542 Family VI. Sporichthyaceae...... 544 Genus I. ...... 544 Order VII. Glycomycetales ord. nov...... 546 Family I. Glycomycetaceae ...... 547 Genus I. Glycomyces ...... 547 Genus II. Stackebrandtia ...... 553 Order VIII. Jiangellales ord. nov...... 555 Family I. Jiangellaceae ...... 557 Genus I. Jiangella ...... 557 Genus II. Haloactinopolyspora ...... 560 Order IX. Kineosporiales ord. nov...... 561 Family I. Kineosporiaceae ...... 562 Genus I. Kineosporia ...... 562 Genus II. Kineococcus ...... 565 Genus III. Quadrisphaera ...... 567 Order X. ...... 569 Family I. ...... 571 Genus I. Micrococcus ...... 571 Genus II. Acaricomes ...... 577 Genus III. Arthrobacter ...... 578 Genus IV. Citricoccus ...... 624 Genus V. Kocuria ...... 626 Genus VI. Nesterenkonia ...... 636 Genus VII. Renibacterium ...... 643 Genus VIII. Rothia ...... 646 Genus IX. Yaniella ...... 650 Genus X. Zhihengliuella ...... 653 CONTENTS xiii

Family II. ...... 667 Genus I. Beutenbergia ...... 669 Genus II. Miniimonas ...... 671 Genus III. Salana ...... 673 Genus IV. Serinibacter ...... 677 Family III. Bogoriellaceae ...... 678 Genus I. Bogoriella ...... 679 Genus II. Georgenia ...... 681 Family IV. Brevibacteriaceae ...... 685 Genus I. Brevibacterium ...... 685 Family V. ...... 701 Genus I. Cellulomonas ...... 702 Genus II. Incertae sedis Actinotalea ...... 710 Genus III. Incertae sedis Demequina ...... 712 Genus IV. Oerskovia ...... 713 Genus V. Tropheryma ...... 717 Family VI. Dermabacteraceae...... 727 Genus I. Dermabacter ...... 727 Genus II. Brachybacterium ...... 730 Family VII. ...... 738 Genus I. Dermacoccus ...... 738 Genus II. Demetria ...... 742 Genus III. Kytococcus ...... 744 Family VIII. ...... 748 Genus I. Dermatophilus ...... 749 Genus II. Kineosphaera ...... 752 Family IX. ...... 754 Genus I. Intrasporangium ...... 759 Genus II. Arsenicicoccus ...... 761 Genus III. Humihabitans ...... 764 Genus IV. Janibacter ...... 765 Genus V. Knoellia ...... 769 Genus VI. Kribbia ...... 773 Genus VII. Lapillicoccus ...... 774 Genus VIII. Ornithinicoccus ...... 775 Genus IX. Ornithinimicrobium ...... 777 Genus X. Oryzihumus ...... 781 Genus XI. Phycicoccus ...... 782 Genus XII. Serinicoccus ...... 786 Genus XIII. Terrabacter ...... 788 Genus XIV. Terracoccus ...... 790 Genus XV. Tetrasphaera ...... 792 Family X. Jonesiaceae ...... 802 Genus I. Jonesia ...... 802 Family XI. ...... 807 Genus I. Microbacterium ...... 814 Genus II. Agreia ...... 852 Genus III. Agrococcus ...... 855 Genus IV. Agromyces ...... 862 Genus V. Clavibacter ...... 877 Genus VI. Cryobacterium ...... 883 Genus VII. Curtobacterium ...... 887 Genus VIII. Frigoribacterium ...... 895 Genus IX. Frondihabitans ...... 898 xiv CONTENTS

Genus X. Gulosibacter ...... 900 Genus XI. Humibacter ...... 904 Genus XII. Labedella ...... 906 Genus XIII. Leifsonia ...... 907 Genus XIV. Leucobacter ...... 923 Genus XV. Microcella ...... 933 Genus XVI. Microterricola ...... 934 Genus XVII. Mycetocola ...... 936 Genus XVIII. Okibacterium ...... 940 Genus XIX. Phycicola ...... 942 Genus XX. Plantibacter ...... 943 Genus XXI. Pseudoclavibacter ...... 949 Genus XXII. Rathayibacter ...... 953 Genus XXIII. Rhodoglobus ...... 964 Genus XXIV. Salinibacterium ...... 969 Genus XXV. Subtercola ...... 973 Genus XXVI. Yonghaparkia ...... 975 Family XII. ...... 995 Genus I. Promicromonospora ...... 995 Genus II. Cellulosimicrobium ...... 1002 Genus III. Isoptericola ...... 1006 Genus IV. Myceligenerans ...... 1010 Genus V. Xylanibacterium...... 1012 Genus VI. Xylanimicrobium ...... 1015 Genus VII. Xylanimonas ...... 1016 Family XIII. Rarobacteraceae ...... 1019 Genus I. Rarobacter ...... 1020 Family XIV. Ruaniaceae ...... 1022 Genus I. Ruania ...... 1024 Genus II. Haloactinobacterium ...... 1025 Family XV. Sanguibacteraceae ...... 1027 Genus I. Sanguibacter ...... 1030 Part B Order XI. Micromonosporales ord. nov...... 1035 Family I. ...... 1035 Genus I. Micromonospora ...... 1039 Genus II. Actinocatenispora ...... 1057 Genus III. Actinoplanes ...... 1058 Genus IV. Asanoa ...... 1088 Genus V. Catellatospora ...... 1090 Genus VI. Catenuloplanes ...... 1092 Genus VII. Couchioplanes ...... 1094 Genus VIII. Dactylosporangium ...... 1096 Genus IX. Krasilnikovia...... 1106 Genus X. Longispora ...... 1107 Genus XI. Luedemannella ...... 1110 Genus XII. Pilimelia ...... 1111 Genus XIII. Polymorphospora ...... 1117 Genus XIV. Salinispora ...... 1118 Genus XV. Spirilliplanes ...... 1123 Genus XVI. Verrucosispora ...... 1124 Genus XVII. Virgisporangium ...... 1127 Order XII. ord. nov...... 1137 Family I. ...... 1138 Genus I. Propionibacterium ...... 1138 CONTENTS xv

Genus II. Aestuariimicrobium ...... 1155 Genus III. Brooklawnia ...... 1156 Genus IV. Friedmanniella ...... 1159 Genus V. Granulicoccus ...... 1165 Genus VI. Luteococcus...... 1166 Genus VII. Microlunatus ...... 1168 Genus VIII. Micropruina ...... 1173 Genus IX. Propionicicella ...... 1174 Genus X. Propionicimonas ...... 1175 Genus XI. Propioniferax ...... 1177 Genus XII. Propionimicrobium ...... 1179 Genus XIII. Tessaracoccus ...... 1180 Family II. Nocardioidaceae ...... 1189 Genus I. Nocardioides ...... 1197 Genus II. Actinopolymorpha ...... 1251 Genus III. Aeromicrobium ...... 1258 Genus IV. Kribbella ...... 1268 Genus V. Marmoricola ...... 1284 Order XIII. Pseudonocardiales ord. nov...... 1301 Family I. ...... 1302 Genus I. Pseudonocardia ...... 1305 Genus II. Actinoalloteichus ...... 1323 Genus III. Actinokineospora ...... 1325 Genus IV. Actinosynnema ...... 1331 Genus V. Amycolatopsis ...... 1334 Genus VI. Crossiella ...... 1359 Genus VII. Goodfellowiella ...... 1363 Genus VIII. Kibdelosporangium ...... 1366 Genus IX. Kutzneria ...... 1371 Genus X. Lechevalieria ...... 1375 Genus XI. Lentzea ...... 1379 Genus XII. Prauserella ...... 1384 Genus XIII. Saccharomonospora ...... 1390 Genus XIV. ...... 1396 Genus XV. Saccharothrix ...... 1415 Genus XVI. Streptoalloteichus ...... 1419 Genus XVII. Thermocrispum ...... 1423 Genus XVIII. Umezawaea ...... 1427 Order XIV. Streptomycetales ord. nov...... 1446 Family I. ...... 1446 Genus I. Streptomyces ...... 1455 Genus Incertae sedis I. Kitasatospora ...... 1768 Genus Incertae sedis II. Streptacidiphilus ...... 1777 Order XV. ord. nov...... 1805 Family I. ...... 1807 Genus I. Streptosporangium ...... 1811 Genus II. Acrocarpospora ...... 1825 Genus III. Herbidospora ...... 1827 Genus IV. Microbispora ...... 1831 Genus V. Microtetraspora ...... 1838 Genus VI. Nonomuraea ...... 1844 Genus VII. Planobispora ...... 1861 Genus VIII. Planomonospora ...... 1866 Genus IX. Planotetraspora ...... 1873 Genus X. Sphaerisporangium ...... 1875 Genus XI. Thermopolyspora ...... 1880 xvi CONTENTS

Family II. Nocardiopsaceae ...... 1889 Genus I. Nocardiopsis ...... 1891 Genus II. Haloactinospora ...... 1907 Genus III. Streptomonospora ...... 1908 Genus IV. Thermobifida ...... 1914 Family III. ...... 1929 Genus I. Thermomonospora ...... 1931 Genus II. Actinocorallia ...... 1935 Genus III. ...... 1940 Genus IV. Spirillospora ...... 1959 Order XVI. Incertae sedis ...... 1967 Genus I. Thermobispora ...... 1967 Class II. Acidimicrobiia class. nov ...... 1968 Order I. Acidimicrobiales ...... 1969 Family I. Acidimicrobiaceae ...... 1970 Genus I. Acidimicrobium ...... 1970 Genus II. Ferrimicrobium ...... 1972 Genus III. Ferrithrix ...... 1973 Family II. Iamiaceae ...... 1974 Genus I. Iamia ...... 1975 Class III. Coriobacteriia class. nov...... 1975 Order I. Coriobacteriales ...... 1976 Family I. Coriobacteriaceae ...... 1977 Genus I. Coriobacterium ...... 1977 Genus II. Atopobium ...... 1978 Genus III. Collinsella ...... 1984 Genus IV. Cryptobacterium ...... 1987 Genus V. Denitrobacterium ...... 1988 Genus VI. Eggerthella ...... 1990 Genus VII. Olsenella ...... 1993 Genus VIII. Slackia ...... 1995 Class IV. Nitriliruptoria class. nov...... 2000 Order I. Nitriliruptorales ...... 2001 Family I. Nitriliruptoraceae ...... 2001 Genus I. Nitriliruptor ...... 2001 Order II. Euzebyales ...... 2002 Family I. Euzebyaceae ...... 2003 Genus I. Euzebya ...... 2003 Class V. Rubrobacteria class. nov...... 2004 Order I. Rubrobacterales ...... 2005 Family I. Rubrobacteraceae ...... 2006 Genus I. Rubrobacter ...... 2006 Class VI. Thermoleophilia class. nov...... 2010 Order I. Thermoleophilales ...... 2010 Family I. Thermoleophilaceae ...... 2011 Genus I. Thermoleophilum ...... 2011 Order II. Solirubrobacterales ...... 2014 Family I. Solirubrobacteraceae ...... 2015 Genus I. Solirubrobacter ...... 2015 Family II. Conexibacteraceae ...... 2018 Genus I. Conexibacter ...... 2019 Family III. Patulibacteraceae ...... 2024 Genus I. Patulibacter ...... 2024

Author index...... 2029

Index of scientific names of Archaea and ...... 2031 Contributors

Hiroshi Akasaka Bruno Biavati Creative Research Initiative “Sousei” (CRIS), Hokkaido Department of Agricultural Sciences, Bologna University, University, Kita 21, Nishi 10, Kita-ku, Sapporo 001-0021, Viale Fanin 42, 40127 Bologna, Italy Japan [email protected] Vladimir N. Akimov Sandra Buczolits VKM – All-Russian Collection of Microorganisms, Institut für Bakteriologie, Mykologie und Hygiene, G.K. Skryabin Institute of Biochemistry and Physiology Veterinärmedizinische Universität Wien, Veterinärplatz 1, of Microorganisms, Russian Academy of Sciences, A-1210 Wien, Austria Pushchino, Moscow Region 142290, Russia [email protected] [email protected] Hans-Jürgen Busse Robin C. Anderson Institut für Bakteriologie, Mykologie und Hygiene, Research Microbiologist/Lead Scientist, Veterinärmedizinische Universität Wien, Veterinärplatz 1, United States Department of Agriculture, A-1210 Wien, Austria Southern Plains Agricultural Research Center, [email protected] Food and Feed Safety Research Unit, 2881 F&B Road, W. Ray Butler College Station, TX 77845, USA Division of Elimination, National Center for HIV, [email protected] STD and Tuberculosis Prevention, Centers for Disease Control Elena V. Ariskina and Prevention, Atlanta, GA, USA VKM – All-Russian Collection of Microorganisms, [email protected] G.K. Skryabin Institute of Biochemistry and Physiology Lorena Carro of Microorganisms, Russian Academy of Sciences, Pushchino, Departamento de Microbiología y Genética, Moscow Region 142290, Russia Edificio Departamental, Lab. 205, Campus Unamuno, [email protected] Universidad de Salamanca, 37007 Salamanca, Spain Brian Austin [email protected] Institute of Aquaculture, School of Natural Sciences, Linda Cavaletti University of Stirling, Stirling FK9 4LA, Scotland, UK Fondazione Istituto Insubrico di Ricerca per la Vita, [email protected] via Robert Lepetit 34, 21040 Gerenzano, Italy Undine Behrendt [email protected] Leibniz Centre for Agricultural Landscape Research (ZALF), Wen-Feng Chen Institute of Landscape Matter Dynamics, State Key Laboratories of Agrobiotechnology, Eberswalder Straße 84, D-15374 Müncheberg, Germany College of Biological Sciences, China Agricultural University, [email protected] Beijing 100193, P.R. China Yoshimi Benno [email protected] Benno Laboratory, Innovation Center, RIKEN, 2-1 Hirosawa, Matthew D. Collins Wako, Saitama 351-0198, Japan The University of Reading, Whiteknights, [email protected] Reading RG6 6AP, UK David R. Benson Milton S. da Costa Department of Molecular & Cell Biology, Department of Life Sciences, University of Coimbra, University of Connecticut, Storrs, CT 06269-3125, USA 3001-401, Coimbra, Portugal [email protected] [email protected] Kathryn A. Bernard Xiao-Long Cui National Microbiology Laboratory, Public Health Yunnan Institute of Microbiology, Yunnan University, Agency of Canada, 1015 Arlington Street, Winnipeg, Cuihu Beilu 2, Kunming, Yunnan 650091, P.R. China Manitoba R3E 3R2, Canada [email protected] [email protected] Ewald B. M. Denner Alison M. Berry Institut für Bakteriologie, Mykologie und Hygiene, Department of Plant Sciences, One Shields Avenue, Veterinärmedizinische Universität Wien, Veterinärplatz 1, University of California, Davis, CA 95616, USA A-1210 Wien, Austria [email protected] [email protected]

xvii xviii CONTRIBUTORS

Floyd E. Dewhirst Ingrid Groth Department of Molecular Genetics, Molekulare und Angewandte Mikrobiologie, The Forsyth Institute, 245 First Street, Leibniz-Institut für Naturstroff-Forschung Cambridge, MA 02142, USA und Infektionsbiologie e. V., Hans-Knöll-Institut, [email protected] Beutenbergstrasse 11a, D-07745 Jena, Germany Stefano Donadio [email protected] KtedoGen Srl and NAICONS Scrl, Via Fantoli 16/15, Val Hall 20138 Milano, Italy Anaerobe Reference Unit, Public Health Wales Microbiology, [email protected], [email protected] University Hospital of Wales, Cardiff CF14 4XW, UK [email protected] Lubov V. Dorofeeva VKM – All-Russian Collection of Microorganisms, Satoshi Hanada G.K. Skryabin Institute of Biochemistry and Physiology Institute for Biological Resources and Functions, of Microorganisms, Russian Academy of Sciences, National Institute of Advanced Industrial Science Pushchino, Moscow Region 142290, Russia and Technology (AIST), Tsukuba Central 6, 1-1-1 Higashi, [email protected] Tsukuba 305-8566, Japan [email protected] Jean P. Euzéby Ecole Nationale Veterinaire, 23 chemin des Capelles, Lesley Hoyles B.P. 87614, 31076 Toulouse cedex 3, France Microbial Ecology & Health Group, [email protected] Department of Food & Nutritional Sciences, University of Reading, Whiteknights Campus, Reading, UK Lyudmila I. Evtushenko [email protected] VKM – All-Russian Collection of Microorganisms, Wael N. Hozzein G.K. Skryabin Institute of Biochemistry and Physiology Botany Department, Faculty of Science, Beni-Suef University, of Microorganisms, Russian Academy of Sciences, Pushchino, Beni-Suef, Egypt Moscow Region 142290, Russia [email protected] [email protected] Ying Huang José F. Fernández-Garayzábal State Key Laboratory of Microbial Resources, Departamento de Sanidad Animal, Institute of Microbiology, Chinese Academy of Sciences, Facultad de Veterinaria, Universidad Complutense, No. 1 West Beichen Road, Chaoyang District, Beijing 100101, 28040 Madrid, Spain P.R. China [email protected] [email protected] Christopher Franco Paul R. Jensen Department of Medical Biotechnology, School of Medicine, Scripps Institution of Oceanography, University of California Flinders University, Bedford Park, South Australia 5042, San Diego, La Jolla, CA 92093-0204, USA Australia [email protected] chris.franco@flinders.edu.au Amanda L. Jones Guido Funke Department of Biology, Food and Nutritional Sciences, Department of Medical Microbiology & Hygiene, School of Life Sciences, A314 Ellison Building, Northumbria Gärtner & Colleagues Laboratories, Elisabethenstrasse 11, University, Newcastle upon Tyne NE1 8ST, UK D-88212 Ravensburg, Germany [email protected] [email protected] Akiko Kageyama George M. Garrity Kitasato Institute for Life Sciences, Kitasato University, Department of Microbiology, Michigan State University, 5-9-1 Shirokane, Minato-ku, Tokyo 108-8641, Japan 6162 Biomedical and Physical Sciences Building, [email protected] East Lansing, MI 48824-4320, USA Peter Kämpfer [email protected] Institut für Angewandte Mikrobiologie, Olga Genilloud Justus-Liebig-Universität Giessen, Heinrich-Buff-Ring Fundación MEDINA, Avda del Conocimiento 3, 26-32 (IFZ), D-35392 Giessen, Germany Parque Tecnológico Ciencias de la Salud, 18100 Armilla, [email protected] Granada, Spain Hiroaki Kasai [email protected], [email protected] Marine Biotechnology Institute, 3-75-1, Heita, Kamashi, Michael Goodfellow Iwate 026-0001, Japan School of Biology, Ridley Building, University of Newcastle, [email protected] Newcastle upon Tyne NE1 7RU, UK Ellen M. Kerr [email protected] Science and Advice for Scottish Agriculture, Anthony C. Greene Roddinglaw Road, Edinburgh, EH12 9FJ, Scotland, UK Microbial Gene Research and Resources Facility, Seung Bum Kim School of Biomolecular and Physical Sciences, Department of Microbiology and Molecular Biology, Griffith University, Brisbane, Queensland 4111, Chungnam National University, 220 Gung-dong, Yuseong, Australia Daejeon 305-764, Republic of Korea t.greene@griffith.edu.au [email protected] CONTRIBUTORS xix

Helmut König Matthias Maiwald Institute of Microbiology and Wine Research, Department of Pathology and Laboratory Medicine, Johannes Gutenberg University, Becherweg 15, KK Women’s and Children’s Hospital, 55128 Mainz, Germany 100 Bukit Timah Road, Singapore 229899 [email protected] matthias.maiwald@flinders.edu.au, [email protected] Valentina I. Krausova Luis A. Maldonado VKM – All-Russian Collection of Microorganisms, Instituto de Ciencias del Mar y Limnología (ICMyL), G.K. Skryabin Institute of Biochemistry and Physiology Universidad Nacional Autónoma de México (UNAM), of Microorganisms, Russian Academy of Sciences, Pushchino, 04510 Mexico, DF, Mexico Moscow Region 142290, Russia [email protected] [email protected] Célia Manaia Noel R. Krieg Escola Superior de Biotecnologia, Universidade Católica 617 Broce Drive, Blacksburg, VA 24060-2801, USA Portuguesa, R. Dr António Bernardino de Almeida, [email protected] 4200-072 Porto, Portugal Takuji Kudo [email protected] Japan Collection of Microorganisms, RIKEN, Hirosawa, Wako, Eustoquio Martínez-Molina Saitama 351-0198, Japan Departamento de Microbiología y Genética, [email protected] Edificio Departamental, Lab. 209, Universidad de Salamanca, Yashawant Kumar Salamanca, Spain NCIMB Ltd, Ferguson Building, [email protected] Craibstone Estate, Bucksburn, Aberdeen AB21 9YA, Abdul M. Maszenan Scotland, UK Environmental Engineering Research Centre, David P. Labeda School of Civil and Environmental Engineering, National Center for Agricultural Utilization Research, Nanyang Technological University, 639798, Singapore U.S. Department of Agriculture, Peoria, IL 61604-3999, USA [email protected] [email protected] Pedro F. Mateos Paul A. Lawson Departamento de Microbiología y Genética, Department of Botany and Microbiology, George Lynn Edificio Departamental, Campus Unamuno, Cross Hall, 770 Van Vleet Oval, The University of Oklahoma, Universidad de Salamanca, 37007 Salamanca, Spain Norman, OK 73019-0245, USA [email protected] [email protected] Atsuko Matsumoto Soon Dong Lee Kitasato Institute for Life sciences, Kitasato University, School of Biological Sciences and Research Center 5-9-1 Shirokane, Minato-ku, Tokyo 108-8641, Japan for Molecular Microbiology, Seoul National University, [email protected] Republic of Korea, Seoul, Korea Paola Mattarelli [email protected] Department of Agricultural Sciences, Bologna University, Wen-Jun Li Viale Fanin 42, 40127 Bologna, Italy Key Laboratory of Microbial Diversity in Southwest China, [email protected] Ministry of Education and Laboratory for Conservation Anne L. McCartney and Utilization of Bio-Resources, Yunnan Institute Microbial Ecology and Health Group, Department of Microbiology, Yunnan University, Kunming 650091, of Food and Nutritional Sciences, University of Reading, P.R. China Whiteknights, P.O. Box 226, Reading, RG6 6AP, UK [email protected], [email protected] [email protected] Zhi-Heng Liu Andrew McDowell Institute of Microbiology, Chinese Academy of Sciences, Centre for Infection and Immunity, School of Medicine, P.O. Box 2714, Beijing 100190, P.R. China Dentistry and Biomedical Sciences, Queen’s University Belfast, [email protected] Medical Biology Centre, 97 Lisburn Road, Belfast BT9 7BL, UK Nicole Lodders [email protected] Institut für Angewandte Mikrobiologie, Simon J. McIlroy Justus-Liebig-Universität Giessen, Heinrich-Buff-Ring Biotechnology Research Centre, La Trobe University, 26-32 (IFZ), D-35392 Giessen, Germany P.O. Box 199, Bendigo, Victoria 3550, Australia [email protected] [email protected] Wolfgang Ludwig Patricia Messenberg Guimarães Lehrstuhl für Mikrobiologie, Technische Universität Embrapa Genetic Resources and Biotechnology, München, Emil-Ramann-Str. 4, D-85350 Freising, Germany PqEB Final W3 Norte, P.O. Box 02372, 70770-900 Brasília-DF, [email protected] Brazil John G. Magee [email protected] HPA Microbiology Services Newcastle Laboratory, William M. Moe Level 2, Freeman Hospital High Heaton, Department of Civil and Environmental Engineering, Newcastle upon Tyne NE7 7DN, UK Louisiana State University, Baton Rouge, LA 70803, USA [email protected] [email protected] xx CONTRIBUTORS

Paolo Monciardini Erika T. Quintana KtedoGen srl, via Fantoli 16/15, 20138 Milano, Italy Instituto Politécnico Nacional (IPN), Escuela Nacional [email protected] de Ciencias Biológicas (ENCB), Department of Microbiology, Kazunori Nakamura General Microbiology Laboratory, Prolongación de Carpio Institute for Biological Resources and Functions, y Plan de Ayala s/n, Col. Santo Tomás, Deleg. Miguel Hidalgo, National Institute of Advanced Industrial Science C.P. 11340, Mexico City, Mexico and Technology (AIST), Tsukuba, Ibaraki, Japan [email protected] [email protected] Fred A. Rainey Futoshi Nakazawa Department of Biological Sciences, University of Alaska Department of Oral Microbiology, School of Dentistry, Anchorage, Providence Drive, Anchorage, AK 99508, USA Health Sciences University of Hokkaido, [email protected] 1757 Kanazawa, Tobetsu-Ishikari, Hokkaido, 061-0293, David A. Relman Japan Departments of Medicine, and of Microbiology [email protected] & Immunology, Stanford University School of Medicine, Olga I. Nedashkovskaya Stanford, CA 94305-5124, USA Pacific Institute of Bioorganic Chemistry, [email protected] of the Far-Eastern Branch of the Russian Raúl Rivas Academy of Sciences, Pr. 100 let Vladivostoku 159, Departamento de Microbiología y Genética, 690022, Vladivostok, Russia Edificio Departamental, Lab. 209, Campus Unamuno, [email protected], [email protected] Universidad de Salamanca, 37007 Salamanca, Spain Balbina Nogales [email protected] Area de Microbiologia, Dept. Biologia, Gerard S. Saddler Universitat de les Illes Balears, Crtra. Valldemossa km 7.5, Science and Advice for Scottish Agriculture, Roddinglaw Road, 07122 Palma de Mallorca, Spain Edinburgh, EH12 9FJ, Scotland, UK [email protected] [email protected] Philippe Normand Klaus P. Schaal IFR41 CNRS Ecologie Genetique Evolution, UMR 5557 Institut für Medizinische Mikrobiologie, CNRS Ecologie Microbienne, Université Claude-Bernard Immunologie und Parasitologie, Universitätsklinikum Bonn, Lyon1, Bat G. Mendel, 43 Blvd du 11 novembre 1918, Sigmund-Freud-Strasse 25, D-53105 Bonn, Germany 69622 Villeurbanne Cedex, France [email protected], [email protected] [email protected] Jenny Schäfer Paul R. Norris Bundesanstalt für Arbeitsschutz und Arbeitsmedizin, School of Life Sciences, University of Warwick, “Biologische Arbeitsstoffe”, Nöldnerstrasse 40–42, Coventry CV4 7AL, UK 10317 Berlin, Germany [email protected] [email protected] Olga C. Nunes Peter Schumann LEPAE-Departamento de Engenharia Química, Faculdade de Engenharia, Universidade do Porto, DSMZ – Deutsche Sammlung von Mikroorganismen R. Dr Roberto Frias, Porto, 4200-465, Portugal und Zellkulturen, Inhoffenstraße 7 B, 38124 Braunschweig, [email protected] Germany [email protected] Cristina Pascual National Documentation Centre, 48 Vas. Constantinou Susmitha Seshadri Avenue, GR11635 Athens, Greece Department of Microbiology, University of Georgia, [email protected], [email protected] 527 Biological Sciences Building, Cedar Street, Athens, GA 30602, USA Bharat K. C. Patel [email protected] Microbial Discovery Research Unit, School of Biomolecular and Physical Sciences, Griffith University, Nathan Campus, Robert J. Seviour Kessels Road, Brisbane, Queensland 4111, Australia Biotechnology Research Centre, La Trobe University, b.patel@griffith.edu.au P.O. Box 199, Bendigo, Victoria 3550, Australia [email protected] Sheila Patrick Centre for Infection and Immunity, School of Medicine, Peter P. Sheridan Dentistry and Biomedical Sciences, Queen’s University Belfast, Department of Biological Sciences, Idaho State University, Medical Biology Centre, 97 Lisburn Road, Belfast BT9 7BL, P.O. Box 8007, Pocatello, ID 83209, USA UK [email protected] [email protected] Jacques A. Soddell Jerome J. Perry (Deceased) Cajid Media, 21 Wirth Street, Bendigo, Victoria 3550, 3125 Eton Road, Raleigh, NC 27608, USA Australia [email protected] Rüdiger Pukall DSMZ – Deutsche Sammlung von Mikroorganismen Cathrin Spröer und Zellkulturen, Inhoffenstraße 7 B, 38124 Braunschweig, DSMZ – Deutsche Sammlung von Mikroorganismen Germany und Zellkulturen, Inhoffenstraße 7 B, 38124 Braunschweig, [email protected] Germany [email protected] CONTRIBUTORS xxi

Erko Stackebrandt Atsuko Ueki 40 Rue des Ecoles, 75005 Paris, France Faculty of Agriculture, Yamagata University, [email protected] Wakaba-machi 1-23, Tsuruoka 997-8555, Japan Thaddeus B. Stanton [email protected] Agricultural Research Service – Midwest Area, Katuji Ueki National Animal Disease Center, United States Department Faculty of Agriculture, Yamagata University, of Agriculture, P.O. Box 70, 1920 Dayton Avenue, Wakaba-machi 1-23, Tsuruoka 997-8555, Japan Building 24, Ames, IA 50010-0070, [email protected] USA Andreas Ulrich [email protected] Institute of Landscape Matter Dynamics, Leibniz-Centre Virginie Storms for Agricultural Landscape Research (ZALF) e.V., Lab. voor Microbiologie en Microbiele Genetica, Eberswalder Strasse 84, D-15374 Müncheberg, Germany Faculteit Wetenschappen, Univeristeit of Gent, [email protected] K.L. Ledeganckstraat 35, B-9000 Ghent, Belgium Peter Vandamme [email protected] Laboratorium voor Microbiologie, Faculteit Wetenschappen, Ken-ichiro Suzuki Universiteit Gent, Ledeganckstraat 35, B-9000 Gent, Belgium NITE Biological Resource Center (NBRC), [email protected] National Institute of Technology and Evaluation, Encarna Velázquez 2-5-8, Kazusakamatari 2-chome, Kisarazu-shi, Chiba 292-0818, Departmento de Microbiología y Genética, Lab 209, Japan Edificio Departamental, Universidad de Salamanca, [email protected] Campus Miguel de Unamuno, 37007 Salamanca, Spain Yo¯ko Takahashi [email protected] Kitasato Institute for Life Sciences, Kitasato University, António Veríssimo 5-9-1 Shirokane, Minato-ku, Tokyo 108-8641, Japan Centro de Neurociências e Biologia Celular and Department [email protected] of Life Sciences, University of Coimbra, Apartado 3046, Mariko Takeuchi 3001-401 Coimbra, Portugal Takeda Chemical Industries, 17-85, Juso-honmachi, 2-chome, [email protected] Yodogawa-ku, Osaka 532-8686, Japan Gernot Vobis Departamento de Botánica, Centro Regional Universitario Tomohiko Tamura Bariloche, Universidad Nacional del Comahue, Quintral, NITE Biological Resource Center (NBRC), 1250 8400 San Carlos de Bariloche, Prov. de Río Negro, National Institute of Technology and Evaluation, Argentina 2-5-8, Kazusakamatari, Kisarazu-shi, [email protected] Chiba 292-0818, Japan [email protected] William G. Wade Microbiology, King’s College London Dental Institute, Geok Yuan Annie Tan Floor 17, Tower Wing, Guy’s Campus, London SE1 9RT, UK Microbiology Division, Institute of Biological Sciences, [email protected] University of Malaya, 50603 Kuala Lumpur, Malaysia [email protected] Alan C. Ward School of Biology, University of Newcastle upon Tyne, Shu-Kun Tang Newcastle upon Tyne NE1 7RU, UK The Key Laboratory for Microbial Resources of the Ministry [email protected] of Education, P.R.China, and Laboratory for Conservation and Utilization Bio-Resources, Yunnan Institute of William B. Whitman Microbiology, Yunnan University, Kunming 650091, Department of Microbiology, University of Georgia, P.R. China 527 Biological Sciences Building, Cedar Street, Athens, GA 30602-2605, USA Tian-shen Tao [email protected] College of Life Sciences, Wuhan University, Wuhan 430072, Monika Wieser Hubei Province, P.R. China Institut für Bakteriologie, Mykologie und Hygiene, [email protected] Veterinärmedizinische Universität Wien, Veterinärplatz 1, Martha E. Trujillo A-1210 Wien, Austria Departamento de Microbiología y Genética, [email protected] Edificio Departamental, Lab. 205, Campus Unamuno, Atteyet F. Yassin Universidad de Salamanca, 37007 Salamanca, Institut für Medizinische Mikrobiologie und Immunologie Spain der Universität Bonn, Sigmund-Freud-Straße 25, 53127 Bonn, [email protected] Germany Takanori Tsukamoto [email protected], [email protected] Plant Protection Division, Food Safety and Akira Yokota Consumer Affairs Bureau, Ministry of Agriculture, Institute of Molecular and Cellular Biosciences, Forestry and Fisheries (MAFF)1-2-1 Kasumigaseki, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-Ku, Chiyoda-ku, Tokyo 100-8950, Japan Tokyo 113-0032, Japan [email protected] [email protected] xxii CONTRIBUTORS

Jung-Hoon Yoon Xiao-Yang Zhi Laboratory of Microbial Function, Korea Research The Key Laboratory for Microbial Resources of the Ministry Institute of Bioscience and Biotechnology (KRIBB), of Education, P.R.China, and Laboratory for Conservation P.O. Box 115, Yusong, Taejon, and Utilization Bio-Resources, Yunnan Institute of South Korea Microbiology, Yunnan University, Kunming 650091, [email protected] P.R. China On using the Manual NOEL R. KRIEG AND GEORGE M. GARRITY

Citation c. Synonyms. In some instances a list of some synonyms used in the past for the same genus is given. Other synonyms The Systematics is a peer-reviewed collection of chapters, con- can be found in the Index Bergeyana or the Supplement to the Index tributed by authors who were invited by the Trust to share their Bergeyana. knowledge and expertise of specific taxa. Citations should refer to the author, the chapter title, and inclusive pages rather than d. Etymology of the name. Etymologies are provided as in to the editors. previous editions, and many (but undoubtedly not all) errors have been corrected. It is often difficult, however, to determine Arrangement of the Manual why a particular name was chosen, or the nuance intended, if As in the previous volumes of this edition, the Manual is the details were not provided in the original publication. Those arranged in phylogenetic groups based upon the analyses of authors who propose new names are urged to consult a Greek the 16S rRNA presented in the introductory chapter “Road and Latin authority before publishing in order to ensure gram- map of the phylum Actinobacteria”. This phylum has been sub- matical correctness and also to ensure that the meaning of the stantially modified since the publication of volume 1 in 2001, name is as intended. reflecting both the availability of more experimental data and e. Salient features. This is a brief resume of the salient fea- a different method of analysis. Since volume 5 includes only tures of the taxon. The most important characteristics are given the phylum Actinobacteria, taxa are arranged by class, order, fam- in boldface. The DNA G+C content is given. ily, genus and . Within each taxon, the nomenclatural type is presented first. Other taxa are presented in alphabetical f. Type species. The name of the type species of the genus order without consideration of degrees of relatedness. is also indicated along with the defining publication(s). g. Further descriptive information. This portion elabo- Articles rates on the various features of the genus, particularly those Each article dealing with a bacterial genus is presented wher- features having significance for systematic bacteriology. The ever possible in a definite sequence as follows: treatment serves to acquaint the reader with the overall biol- ogy of the organisms but is not meant to be a comprehensive a. Name of the genus. Accepted names are in boldface, fol- review. The information is normally presented in the follow- lowed by “defining publication(s)”, i.e. the authority for the ing sequence: name, the year of the original description, and the page on which the taxon was named and described. The superscript AL Colonial morphology and pigmentation indicates that the name was included on the Approved Lists of Growth conditions and nutrition Bacterial Names, published in January 1980. The superscript Physiology and metabolism VP indicates that the name, although not on the Approved Lists Genetics, plasmids, and bacteriophages of Bacterial Names, was subsequently validly published in the Phylogenetic treatment International Journal of Systematic and Evolutionary Microbiology (or Antigenic structure the International Journal of Systematic Bacteriology). Names given Pathogenicity within quotation marks have no standing in nomenclature; as Ecology of the date of preparation of the Manual they had not been h. Enrichment and isolation. A few selected methods are validly published in the International Journal of Systematic and Evo- presented, together with the pertinent media formulations. lutionary Microbiology, although they may have been “effectively published” elsewhere. Names followed by the term “nov.” are i. Maintenance procedures. Methods used for maintenance newly proposed but will not be validly published until they ap- of stock cultures and preservation of strains are given. pear in a Validation List in the International Journal of Systematic j. Procedures for testing special characters. This portion and Evolutionary Microbiology. Their proposal in the Manual con- provides methodology for testing for unusual characteristics or stitutes only “effective publication”, not valid publication. performing tests of special importance. b. Name of author(s). The person or persons who prepared k. Differentiation of the genus from other genera. Those the Bergey’s article are indicated. The address of each author characteristics that are especially useful for distinguishing the can be found in the list of Contributors at the beginning of the genus from similar or related organisms are indicated here, Manual. usually in a tabular form.

xxiii xxiv ON USING THE MANUAL

l. Taxonomic comments. This summarizes the available similar or related genera, (b) those that differentiate the species information related to taxonomic placement of the genus and in- within the genus, and (c) those that provide additional infor- dicates the justification for considering the genus a distinct taxon. mation about the species (such information not being particu- Particular emphasis is given to the methods of molecular biology larly useful for differentiation). The meanings of symbols are used to estimate the relatedness of the genus to other taxa, where as follows: such information is available. Taxonomic information regarding +, 90% or more of the strains are positive the arrangement and status of the various species within the genus d, 11–89% of the strains are positive follows. Where taxonomic controversy exists, the problems are −, 90% or more of the strains are negative delineated and the various alternative viewpoints are discussed. D, different reactions occur in different taxa (e.g., species of m. Further reading. A list of selected references, usually of a genus or genera of a family) a general nature, is given to enable the reader to gain access to v, strain instability (NOT equivalent to “d”) additional sources of information about the genus. w, weak reaction. nd, not determined or no data. n. Differentiation of the species of the genus. Those char- nr, not reported. acteristics that are important for distinguishing the various spe- These symbols, and exceptions to their use, as well as the cies within the genus are presented, usually with reference to a meaning of additional symbols, are given in footnotes to the table summarizing the information. tables. o. List of species of the genus. The citation of each species is given, followed in some instances by a brief list of objective Use of the Manual for determinative purposes synonyms. The etymology of the specific epithet is indicated. Many chapters have keys or tables for differentiation of the vari- Descriptive information for the species is usually presented in ous taxa contained therein. For identification of species, it is tabular form, but special information may be given in the text. important to read both the generic and species descriptions Because of the emphasis on tabular data, the species descrip- because characteristics listed in the generic descriptions are not tions are usually brief. The type strain of each species is indi- usually repeated in the species descriptions. cated, together with the collection(s) in which it can be found. The index is useful for locating the articles on unfamiliar (Addresses of the various culture collections are given in the ar- taxa or in discovering the current classification of a particular ticle in volume 1 entitled Culture Collections: An Essential Resource taxon. Every bacterial name mentioned in the Manual is listed for Microbiology.) The 16S rRNA gene sequence used in phyloge- in the index. In addition, an up-to-date outline of the taxonomic netic analysis and placement of the species into the taxonomic framework is provided in the introductory chapter “Road map framework is given, along with the GenBank (or other database) of the phylum Actinobacteria”. accession number. Additional comments may be provided to point the reader to other well-characterized strains of the spe- Errors, comments, and suggestions cies and any other known DNA sequences that may be relevant. As in previous volumes, the editors and authors earnestly solicit p. Species incertae sedis. The List of Species may be fol- the assistance of all microbiologists in the correction of possible lowed in some instances by a listing of additional species under errors in Bergey’s Manual of Systematic Bacteriology. Comments on the heading “Species Incertae sedis” or “Other organisms”, etc. the presentation will also be welcomed as well as suggestions for The taxonomic placement or status of such species is question- future editions. Correspondence should be addressed to: able, and the reasons for the uncertainty are presented. Editorial Office q. References. All references given in the article are listed Bergey’s Manual Trust alphabetically at the end of the family chapter Department of Microbiology University of Georgia Tables Athens, GA 30602-2605, USA In each article dealing with a genus, there are generally three Tel: +1-706-542-4219; fax +1-706-542-6599 kinds of table: (a) those that differentiate the genus from e-mail: [email protected] Road map of the phylum Actinobacteria WOLFGANG LUDWIG, JEAN EUZÉBY, PETER SCHUMANN, HANS-JÜRGEN BUSSE, MARTHA E. TRUJILLO, PETER KÄMPFER AND WILLIAM B. WHITMAN

This revised road map and the resulting taxonomic outline has been a continuous debate concerning the justification and update the previous versions of Garrity and Holt (2001) and power of a single marker molecule for elucidating and estab- Garrity et al. (2005) with the description of additional taxa lishing the phylogeny and taxonomy of organisms, respectively. and new phylogenetic analyses. While the road map seeks to Although generally well established in taxonomy, comparable be complete for all taxa validly named prior to 1 January 2008, analyses of multiple genes cannot currently be applied because some taxa described after that date are included. of the lack of comprehensive datasets for other marker mole- The new phylogenetic trees are strict consensus trees based cules. Even in the age of genomics, the datasets for non-rRNA on various maximum-likelihood and maximum-parsimony anal- markers are poor in comparison to more than 400,000 rRNA yses and corrected according to results obtained when apply- primary structures available in general and specialized data- ing alternative treeing methods. Multifurcations indicate that a bases (Cole et al., 2007; Pruesse et al., 2007). Nevertheless, the common branching order was not significantly supported after data provided by full genome sequencing projects have iden- applying alternative treeing approaches. Detailed branching tified a small set of genes representing the conserved core of orders are shown if supported by at least 50% of the “treeings” prokaryotic genomes (Cicarelli et al., 2006; Ludwig and Schle- performed in addition to the maximum-likelihood approach. ifer, 2005). Furthermore, comparative analyses of core gene Given that the focus is on the higher (taxonomic) ranks, sequences globally support the small-subunit rRNA-derived view rather restrictive variability filters were applied. Consequently, of prokaryotic evolution. Although the tree topologies recon- resolution power is lost for lower levels. Of special importance, structed from alternative markers differ in detail, the major relationships within genera lack the resolution that would be groups (and taxa) are verified or at least not disproved (Ludwig obtained with genus/family level analyses. Furthermore, the and Schleifer, 2005). Consequently, this volume is organized on type strain tree, which is available online at www.bergeys.org, is the basis of updated and curated databases of processed small- an extract of comprehensive trees comprising some thousand subunit rRNA primary structures (http://www.arb-silva.de; Lud- sequences. Thus, trees for the specific groups in subsequent wig et al., 2004). chapters, which are based upon smaller datasets and include variable sequence positions, may differ with respect to detailed Data analysis topology, especially at levels of closer relationship within and The current release of the integrated small-subunit rRNA data- between genera. In the trees shown here, branch lengths – in base of the SILVA project (Pruesse et al., 2007) provided the the first instance – indicate significance and only approximate basis for these phylogenetic analyses. The tools of the arb soft- estimated number of substitutions. ware package (Ludwig et al., 2004) were used for data evalu- Starting with the second edition of Bergey’s Manual of Systematic ation, optimization, and phylogenetic inference. A subset of Bacteriology, the arrangement of content follows a phylogenetic about 33,000 high-quality sequences from Bacteria was extracted framework or road map based largely on analyses of nucleotide from the current SILVA SSU Ref database. Among the criteria sequences of the ribosomal small subunit RNA rather than on for restrictive quality analyses and data selection were: cover- phenotypic data (Garrity et al., 2005). Implicit in the use of age of at least positions 18 to 1509 (Escherichia coli 16S rRNA the road map are the convictions that prokaryotes have a phy- numbering), no ambiguities or missing sequence stretches, no logeny and that phylogeny matters. However, phylogenies, like chimeric primary structures, low deviation from overall and other experimentally derived hypotheses, are not static but may group-specific consensus and conservation profiles, and good change whenever new data and/or improved methods of analy- agreement of tree topologies and branch lengths with pro- sis become available (Ludwig and Klenk, 2005). Thus, the large cessed sequence data. Unfortunately, not all of the type strain increases in data since the publication of the taxonomic out- sequences successfully passed this restrictive quality check. The lines in the preceding volumes have led to a re-evaluation of the alignment of the sequences of this subset, as well as all type strain road map. Not surprisingly, the taxonomic hierarchy has been sequences initially excluded given incompleteness or lower quality, modified or newly interpreted for a number of taxonomic units. was manually evaluated and optimized. Phylogenetic treeing was These changes are described in the following paragraphs. first based on the high quality dataset and performed apply- The taxonomic road map proposed in volume 1 and updated ing phylum-specific position filters (50% positional identity). and emended in volume 2 was derived from phylogenetic and The partial or lower quality type strain sequences were subse- principal component analyses of comprehensive datasets of small- quently added using a special arb-tool allowing the optimally subunit rRNA gene sequences. A similar approach is continued positioning of branches to the reference tree without admitting here. Since the introduction of comparative rRNA sequencing topology changes (Ludwig and Klenk, 2005). The consensus (Ludwig and Klenk, 2005; Ludwig and Schleifer, 2005), there trees used for evaluating or modifying the taxonomic outline

1 2 ROAD MAP were based on maximum-likelihood analyses (RAXML, imple- mented in the arb package; Stamatakis et al., 2005) and further evaluated by maximum-parsimony and distance matrix analyses with the respective arb tools (Ludwig et al., 2004). Taxonomic interpretation

In order to ensure applicability and promote acceptance, the "Actinobacteria" proposed taxonomic modifications were made following a conservative procedure. The overall organization follows the type “taxon” principle as applied in the previous volumes. Taxa defined in the outline of the preceding volumes were only uni- fied, dissected, or transferred in the cases of strong phylogenetic support. This approach is justified by the well-known low signifi- cance of local tree topologies (also called “range of unsharp- ness” around the nodes; Ludwig and Klenk, 2005). Thus, many "Nitriliruptoria" of the cases of paraphyletic taxa found were maintained in the "Acidimicrobiia" current road map if the respective (sub)-clusters rooted closely together, even if they were separated by intervening clusters representing other taxa. While reorganization of these taxa "Coriobacteriia" may be warranted, it was not performed in the absence of con- firmatory evidence. The names of type strains of species with "Thermoleophilia" validly published names that are phylogenetically misplaced are also generally maintained. These strains are mentioned in the "Rubrobacteria" context of the respective phylogenetic groups. In case of para- phyly, all concerned species or higher taxa are assigned to the FIGURE 1. Overview of the classes within the phyla Actinobacteria. Con- respective (sub)-groups. New higher taxonomic ranks are only sensus dendrogram of the phylogenetic relationships of the 16S rRNA proposed if species or genera – previously assigned to different genes based on various maximum-likelihood and maximum-parsimony higher taxonomic units – are significantly unified in a mono- analyses and corrected according to results obtained when applying alternative treeing methods. Multifurcations indicate that a common phyletic branch. branching order was not significantly supported after applying alter- Phylum “Actinobacteria” native treeing approaches. Detailed branching orders are shown if supported by at least 50% of the “treeings” performed in addition to The phylum “Actinobacteria” is well supported by analyses of the maximum-likelihood approach. For additional methods, please see the 16S and 23S rRNA genes, presence of conserved insertions the text. and deletions (or indels) in certain proteins, and characteris- tic gene rearrangements (as reviewed by Goodfellow and Fie- dler, 2010). The current road map builds upon the thorough taxonomic analyses of Zhi et al. (2009) and Stackebrandt et al. The proposed classification does not preclude the use of the (1997). However, in the classification proposed herein, the tax- term “actinomycetales” in its conventional sense. This practice onomic ranks of subclass and suborder are not used, and the is common in other prokaryotic groups where the implementa- clades previously represented by these ranks are mostly elevated tion of a natural classification based upon phylogeny made the to the ranks of class and order, respectively. This modification earlier terminology inappropriate. Thus, “bacillus” refers to a makes the taxonomy of the “Actinobacteria” more consistent with member of a large number of genera that encompass aerobic, that of other prokaryotes and thereby facilitates comparisons endospore-forming rods and not the genus Bacillus. between phyla and the development of a unified classifica- With the class “Actinobacteria” defined in this manner, six tion across all bacteria and archaea. Moreover, it reduces the classes are proposed (Figure 1). In addition to the class “Acti- number of subdivisions within the higher ranks from six (class, nobacteria”, which is now restricted to the clades formerly subclass, order, suborder, family, and genus) to four. The lower classified within the subclass , the classes “Acidi- number of higher ranks is more realistic given the limited abil- microbidiia”, “Coriobacteriia”, “Nitriliruptoria”, “Rubrobacteria”, and ity to distinguish phylogenetic relationships among this large “Thermoleophilia” are proposed. This last class includes many of and complex group. This change has a number of important the genera formerly classified within the Rubrobacteria that were consequences. The class “Actinobacteria” now excludes the not closely related to it (see below). subclasses Acidimicrobidae, Coriobacteridae, Nitriliruptoridae, and Class “Actinobacteria” Rubrobacteridae, with the elevation of these subclasses to classes. In addition, with the elevation of suborders to orders, the order As shown in Figure 2, the class “Actinobacteria” comprises the Actinomycetales is now restricted to members of the family Actin- orders previously classified as suborders within the order Actino- omycetaceae and many suborders that are well established in the mycetales by Zhi et al. (2009), as well as Bifidobacteriales, which literature, such as Micrococcineae and Pseudonocardineae, are not was previously classified as an order, and the new order Jian- used. Nevertheless, the possible confusion that might result gellales (Tang et al., 2011). Upon publication of the class “Acti- from these changes is out-weighed by the advantages of a sim- nobacteria”, a type order was not designated. Hence, this name pler classification which more closely resembles that found in is not validly published under Rule 27 of the International Code other prokaryotic phyla. of Nomenclature of Bacteria (Euzéby and Tindall, 2001; Lapage ROAD MAP 3

“Glycomycetales”, “Jiangellales”, “Micromonosporales”, “Propionibac- teriales”, and “Pseudonocardiales”. The second clade includes "Corynebacteriales" the orders Actinomycetales, Bifidobacteriales, “Kineosporiales”, and Micrococcales. The orders “Catenulisporales”, “Streptomycetales”, and “Streptosporangiales” form deep lineages radiating from the base of the class. Lastly, the families of the order “Frankiales” do not form a clade, but appear as independent lineages at the base "Pseudonocardiales" of the tree. However, these relationships were not observed in rRNA gene trees of Zhi et al. (2009). Thus, in the absence of "Actinopolysporales" confirmatory evidence, they were not used to make taxonomic decisions in the road map. "Jiangellales" Order Actinomycetales and family Actinomycetaceae With the elevation of the suborders of Zhi et al. (2009) to "Glycomycetales − Micromonosporales" orders, this order now comprises only the family Actinomyceta- ceae. Thus, the taxonomic designation is no longer congruent "Propionibacteriales" with the common term “actinomycetales”. The family appears as an independent clade somewhat related to the family Jonesi- aceae of the order Micrococcales (Figure 3). It comprises the dif- fuse type genus Actinomyces and the four well-defined genera Actinobaculum, Arcanobacterium, Mobiluncus, and Varibaculum. Actinomycetales − Micrococcales The genus Actinomyces is represented by five clades within the family. The largest clade includes the type species Actinomyces bovis and Actinomyces bowdenii, catuli, dentalis, denticolens, gerenc- seriae, graevenitzii, howellii, israelii, johnsonii, massiliensis, naeslun- Bifidobacteriales dii, oricola, oris, radicidentis, ruminicola, slackii, urogenitalis, and viscosus. The remaining clades are no more closely related to "Kineosporiales" the type species than to the members of other genera within the family, which might be grounds for their reclassification in the future. The second largest clade includes the species Actinomyces canis, cardiffensis, funkei, georgiae, hyovaginalis, meyeri, "Streptomycetales" odontolyticus, radingae, suimastitidis, turicensis, and vaccimaxil- lae. It is loosely related to two additional clades, one of which includes Actinomyces coleocanis and Actinomyces europaeus and the other Actinomyces neuii and the monospecific genus Varibaculum "Catenulisporales" (type species Varibaculum cambriense). With only 90% sequence similarity and some phenotypic differences to Varibaculum, Actinomyces neuii may warrant reclassification in a new genus (Hall et al., 2003). The last clade clusters close to the root of "Streptosporangiales" the family tree and includes Actinomyces marimammalium, hong- kongensis, hordeovulneris, and nasicola. The taxonomic signifi- Sporichthyaceae cance of these groups is discussed in further detail by Schaal and Yassin (2012). Geodermatophilaceae The other genera in the family all form monophyletic clades. Nakamurellaceae "Frankiales" The genera Actinobaculum and Arcanobacterium are related to each other. Actinobaculum comprises the type species Actinobac- Cryptosporangiaceae ulum suis and Actinobaculum massiliense, schaalii, and urinale. Acidothermaceae Arcanobacterium comprises the type species Arcanobacterium hae- Frankiaceae molyticum and Arcanobacterium abortisuis, bernardiae, bialowiezense, bonasi, hippocoleae, phocae, pluranimalium, and pyogenes. The FIGURE 2. Orders of the class Actinobacteria. Analyses were performed genus Mobiluncus comprises the type species Mobiluncus curtisii as described for Figure 1. and Mobiluncus mulieris. This genus has precedence over Falcivi- brio, which appears to be a later heterotypic synonym (Hoyles et al., 1992). Nevertheless, because of its wide use, the name is et al., 2004). adopted for this volume. If so designated by the Judicial Com- Order “Actinopolysporales” and family mission, the type order is likely to be Actinomycetales, which is Actinopolysporaceae the convention followed herein. Within the class, two large clades are observed in the rRNA In the rRNA gene trees described herein, this order is related gene trees prepared for this volume (Figure 2). The first clade to “Corynebacteriales” and “Pseudonocardiales”. These three orders includes the orders “Actinopolysporales”, “Corynebacteriales”, are members of a larger clade that also includes “Glycomycetales”, 4 ROAD MAP

Varibaculum

Mobiluncus

Actinomycetaceae Actinomyces Actinomycetales

Arcanobacterium

Actinobaculum

Jonesiaceae

FIGURE 3. Genera of the order Actinomycetales and Jonesiaceae of the order Micrococcales. Analyses were performed as described for Figure 1.

Bifidobacterium − Gardnerella

Scardovia Parascardovia Alloscardovia Metascardovia Aeriscardovia

FIGURE 4. Genera of the order Bifidobacteriales. Analyses were performed as described for Figure 1.

“Jiangellales”, “Micromonosporales”, and “Propionibacteriales” bifidum; Bifidobacterium adolescentis, angulatum, catenulatum, (Figure 2). In the analyses of Zhi et al. (2009), only the relation- dentium, merycicum, pseudocatenulatum, and ruminantium; Bifi- ship of “Actinopolysporales” and “Glycomycetales” was observed, dobacterium animalis, choerinum, cuniculi, gallicum, magnum, and although without bootstrap support. The monogeneric family pseudolongum; Bifidobacterium asteroides, bombi, coryneforme, indi- comprises the type species Actinopolyspora halophila and Acti- cum, minimum, mongoliense, psychraerophilum, and thermophilum; nopolyspora mortivallis. The species Actinopolyspora iraqiensis was Bifidobacterium boum and thermacidophilum; Bifidobacterium breve, misclassified and is now classified as a heterotypic synonym of longum, and subtile; Bifidobacterium gallinarum, pullorum, and Saccharomonospora halophila. saeculare; Bifidobacterium scardovii; and Bifidobacterium tsurumi- ense. The significance of these subclades is not certain and they Order Bifidobacteriales and family Bifidobacteriaceae only correspond imperfectly to similarities in cell-wall composi- The order Bifidobacteriales comprises the family Bifidobacteriaceae, tion and in 16S–23S intergenic spacer regions (Biavati and Mat- which encompasses seven closely related genera (Figure 4). In tarelli, 2012; Leblond-Bourget et al., 1996). the rRNA gene trees used here, the entire group is separated by a long branch that arises within a clade formed by the Actinomyc- Order “Catenulisporales” and families Catenulisporaceae etales, Micrococcales, and “Kineosporiales” (Figure 2). However, the and Actinospicaceae root of the order Bifidobacteriales is unstable and this relation- This order represents a deep clade within the class “Actinobac- ship was not observed by Zhi et al. (2009). In their gene trees, teria” and comprises two monogeneric families (Figure 5). The based upon a different method of analysis, the order Bifidobac- family Catenulisporaceae contains the type species Catenulispora teriales appears as a deep branch of the class “Actinobacteria”. In acidiphila and three related species, Catenulispora rubra, subtrop- either case, both methods agree that the genera assigned to this ica, and yoronensis. The family Actinospicaceae includes the type group are well separated from other orders. species Actinospica robiniae and Actinospica acidiphila. The family Bifidobacteriaceae comprises two clades. One clade includes the genus Bifidobacterium and the monospecific genus Order “Corynebacteriales” Gardnerella (type species Gardnerella vaginalis). The second In the rRNA gene trees described herein, this order is related clade comprises five additional monospecific genera with type to the orders “Actinopolysporales” and “Pseudonocardiales”. In the species Aeriscardovia aeriphila, Alloscardovia omnicolens, Metascar- analyses of Zhi et al. (2009), only the relationship between dovia criceti, Parascardovia denticolens, and Scardovia inopinata. “Corynebacteriales” and “Pseudonocardiales” was observed, albeit The genus Bifidobacterium encompasses nine subclades, each without bootstrap support. All three orders have the cell-wall about as related to one another as they are to Gardnerella vagi- chemotype IV, which includes the presence of meso-diamin- nalis. These subclades include the type species Bifidobacterium opimelate, arabinose, and galactose. However, their quinones ROAD MAP 5

Bifidobacteriales − Actinomycetales − Micrococcales

Kineosporia

Quadrisphaera Kineosporiaceae − "Kineosporiales"

Kineococcus

Streptacidiphilus

Kitasatospora Streptomycetaceae − "Streptomycetales"

Streptomyces

Catenulispora − Catenulisporaceae "Catenulisporales" Actinospica − Actinospicaceae

FIGURE 5. Genera and families of the orders “Catenulisporales”, “Kineosporiales”, and “Streptomycetales”. Analyses were performed as described for Figure 1.

and major fatty acids are different, and species belonging to the Family Corynebacteriaceae “Pseudonocardiales” lack mycolic acids. Therefore, the biological This family comprises the large and complex genus Corynebacte- importance of this deep relationship requires further examina- rium and the monospecific genus Turicella (type species Turicella tion. These orders are also members of the larger clade that otitidis). On the basis of the rRNA gene tree, many of the species also includes “Glycomycetales”, “Jiangellales”, “Micromonosporales”, of the genus appear equally related to the type species Coryne- and “Propionibacteriales”, whose biological significance is also bacterium diphtheriae and Turicella otitidis and, on this basis, the not known (Figure 2). genus is paraphyletic. However, most Corynebacterium species Six suprageneric taxa can be recognized in the current 16S possess mycolic acids and the menaquinones MK-8(H ), MK- rRNA gene tree, the families Corynebacteriaceae, Dietziaceae, Myco- 2 9(H2), or a mixture of both. Turicella and some Corynebacterium bacteriaceae, Nocardiaceae, Segniliparaceae, and Tsukamurellaceae species, such as Corynebacterium amycolatum, lack mycolic acids. (Figure 6). While most of these families are monophyletic, Turicella also possesses the menaquinones MK-10 and MK-11 many of the genera of the Nocardiaceae appear as deep lineages (Goodfellow and Jones, 2012). It appears that these species in the rRNA gene tree, no more closely related to the type have lost the capacity to produce mycolic acids, so the signifi- genus Nocardia than members of other families (see below). cance of this chemotaxonomic marker is ambiguous. Given the For that reason, this family appears to be paraphyletic. While uncertainties in the relationships within this group, the current the status of some of the families, notably the Mycobacteriaceae taxonomy is retained at this time. and Tsukamurellaceae, is strongly supported by chemotaxonomic In addition to the type species, the genus Corynebacterium data, others such as the family Nocardiaceae are markedly het- comprises a large number of species which, while related to erogeneous in this respect. Indeed, a case can be made for the Corynebacterium diphtheriae, do not form specific associations recognition of the family Gordoniaceae to encompass the gen- with other species of the genus. These include Corynebacterium era Gordonia, Millisia, Williamsia, and Skermania (Goodfellow accolens, aquilae, argentoratense, atypicum, auris, camporealensis, and Jones, 2012). The assignment of the recently described, capitovis, caspium, confusum, doosanense, felinum, flavescens, freibur- mycolateless genera Amycolicicoccus (Wang et al., 2010), Hoyo- gense, halotolerans, kutscheri, lipophiloflavum, lubricantis, macgin- sella (Jurado et al., 2009), and Tomitella (Katayama et al., 2010) leyi, maris, massiliense, mastitidis, mycetoides, renale, spheniscorum, further complicates the delineation of families classified in the testudinoris, timonense, tuberculostearicum, and vitaeruminis. In order Corynebacteriales (Goodfellow and Jones, 2012). Conse- addition, the rRNA gene tree identifies nine small clades of spe- quently, the biological significance of several families within cies, including: Corynebacterium afermentans, appendicis, coyleae, this order requires further study. 6 ROAD MAP

Family Dietziaceae

Mycobacterium − Mycobacteriaceae This monogeneric family comprises the type species Dietzia maris and the closely related species Dietzia aerolata, cercidiphylli, cinnamea, kunjamensis, natronolimnaea, papillomatosis, psychralcal- iphila, schimae, and timorensis. Tsukamurella − Tsukamurellaceae Family Mycobacteriaceae This monogeneric family is well-defined in the 16S rRNA gene tree and also characterized by the presence of mycolic acids Corynebacteriaceae with large numbers of carbon atoms and the predominance of dihydrogenated menaquinones with nine isoprene units (Magee and Ward, 2012). It comprises the type species Myco- Dietzia − Dietziaceae bacterium tuberculosis and over 140 other species with validly pub- lished names. In the 16S rRNA gene tree, a major clade is easily recognized that corresponds to most of the “slow-growing spe- Rhodococcus cies” (Magee and Ward, 2012). This clade is of special impor- tance because it includes many dangerous pathogens, as well as Gordonia the type species Mycobacterium tuberculosis. Other species include Mycobacterium africanum, arosiense, asiaticum, avium, bohemicum, botniense, bouchedurhonense, bovis, branderi, caprae, celatum, chi- Williamsia maera, colombiense, conspicuum, cookii, florentinum, gastri, genavense, Millisia gordonae, haemophilum, heckeshornense, heidelbergense, interjectum, Nocardiaceae intermedium, intracellulare, kansasii, kubicae, kyorinense, lacus, lenti- Skermania flavum, leprae, malmoense, mantenii, marinum, marseillense, microti, montefiorense, nebraskense, noviomagense, palustre, parascrofulaceum, Smaragdicoccus paraseoulense, parmense, pinnipedii, pseudoshottsii, riyadhense, sas- katchewanense, scrofulaceum, seoulense, shimoidei, shottsii, simiae, sto- matepiae, szulgai, triplex, ulcerans, vulneris, and xenopi. A second, Nocardia unrelated clade is composed of other “slow-growing species”: Mycobacterium arupense, hiberniae, kumamotonense, nonchromogeni- cum, and terrae. Most of the remaining species, including most Segniliparus − Segniliparaceae of the “rapid-growing species”, are poorly differentiated from each other in the 16S rRNA gene tree. FIGURE 6. Genera and families of the order “Corynebacteriales”. Analy- Family Nocardiaceae ses were performed as described for Figure 1. In the current rRNA gene tree, the family Nocardiaceae is para- phyletic and is represented by seven genera comprising five deep lineages, none of which are more closely related to each other than to other members of the order “Corynebacteriales”. glaucum, imitans, mucifaciens, riegelii, sundsvallense, thomssenii, In the previous road map, the family contained only the gen- tuscaniense, and ureicelerivorans; Corynebacterium ammoniagenes, era Nocardia and Rhodococcus (Garrity et al., 2005). Gordonia and casei, and stationis; Corynebacterium amycolatum, freneyi, hansenii, Skermania were classified within the family Gordoniaceae and Wil- sphenisci, sputi, ulceribovis, and xerosis; Corynebacterium aurimu- liamsia was classified within the family “Williamsiaceae”. Zhi et al. cosum, minutissimum, phocae, simulans, and singulare; Corynebac- (2009) subsequently proposed combining all these genera and terium auriscanis, bovis, falsenii, jeikeium, kroppenstedtii, resistens, Millisia into a single family Nocardiaceae based upon the rRNA suicordis, terpenotabidum, urealyticum, and variabile; Corynebacte- gene signature nucleotides. With the addition of Smaragdicoccus rium callunae, efficiens, and glutamicum; Corynebacterium ciconiae, (Adachi et al., 2007), this taxonomy was used here. propinquum, and pseudodiphtheriticum; Corynebacterium cystitidis, Chemotaxonomic criteria provide some modest support glucuronolyticum, and pilosum; and Corynebacterium durum, matru- for combining these genera in a single family. Smaragdicoccus chotii, pseudotuberculosis, and ulcerans. possesses cyclic menaquinones, MK-8(H4, Z-methylenecycl)

The affiliations of some additional species of the genus are and MK-8(H4, dicycl), which are similar in structure to those uncertain. Corynebacterium ilicis was originally thought to be a of the genera Nocardia and Skermania, which are dominated homotypic synonym of Arthrobacter ilicis. However, this appears by MK-8(H4, Z-cycl). This feature is distinctive enough to sug- not to be the case and the rRNA gene sequence of Corynebac- gest a close relationship between these genera. Likewise, both terium ilicis is not known (Judicial Commission of the Interna- Gordonia and Williamsia contain the menaquinone MK-9(H2), tional Committee on Systematics of Bacteria, 2008). The type which is consistent with their close relationship in the rRNA strain of has been lost and this species gene tree. In contrast, Rhodococcus and Millisia both possess MK- might be declared nomen dubium (Coyle et al., 1993). Lastly, 8(H2) even though the rRNA gene trees do not indicate a spe- Corynebacterium beticola appears to be more properly classified as cial affinity between them. Therefore, while the menaquinone a strain of Erwinia herbicola (Collins and Jones, 1982). composition supports the hypothesis that some members of this ROAD MAP 7 group are related to each other, it does not provide strong sup- erythropolis, fascians, globerulus, imtechensis, jialingiae, jostii, kore- port that they represent a single family. Somewhat clearer evi- ensis, kyotonensis, maanshanensis, marinonascens, opacus, percolatus, dence for the placement of these seven genera in a single family qingshengii, tukisamuensis, wratislaviensis, and yunnanensis. Lastly, comes from similarities in their mycolic acids. Nocardia species a number of species are not resolved into clades and may rep- contain mycolic acids with 46–64 C-atoms, and Rhodococcus spe- resent new genera. These include Rhodococcus corynebacterioides, cies contain mycolic acids with 30–54 C-atoms. The other five equi, kroppenstedtii, kunmingensis, rhodnii, and triatomae. The case genera all have mycolic acids with numbers of C-atoms within for the recognition of a new genus for is espe- these ranges. Lastly, all genera within this family possess meso- cially strong (Jones and Goodfellow, 2012). diaminopimelate, but this feature is also common to other The monospecific genera Skermania (type species Skermania families of the “Corynebacteriales” and to other orders, such as piniformis) and Smaragdicoccus (type species Smaragdicoccus nii- the “Pseudonocardiales”. In conclusion, the chemotaxonomic gatensis) represent two deep lineages at the base of the rRNA markers are evidence of additional phylogenetic relatedness gene tree of the family Nocardiaceae (Figure 6). not apparent in the rRNA gene tree and offer some support for The genus Williamsia forms a well-defined clade that is the current classification. Nevertheless, the composition of the closely related Gordonia. It is represented by the type species family Nocardiaceae should be considered tentative until a time Williamsia muralis and Williamsia deligens, marianensis, maris, and when conclusive evidence is available. serinedens. In the rRNA gene tree, the genus Nocardia forms a deep, monophyletic lineage near the base of the “Corynebacteriales”. Family Segniliparaceae The Nocardia tree itself exhibits a complicated branching pat- This monogeneric family is represented by the type species Seg- tern with many very short branches. Three clusters can be rec- niliparus rotundus and Segniliparus rugosus. These species form a ognized. The first cluster contains the type species Nocardia deep lineage at the base of the radiation including the Nocar- asteroides and a large number of species whose relatedness is not diaceae and “Corynebacteriales” (Figure 6). well differentiated: Nocardia abscessus, acidivorans, alba, altami- rensis, anemiae, blacklockiae, brasiliensis, caishijiensis, concava, cras- Family Tsukamurellaceae sostreae, cyriacigeorgica, exalbida, gamkensis, harenae, inohanensis, iowensis, jejuensis, jiangxiensis, lijiangensis, mexicana, miyunensis, This monogeneric family comprises the type species Tsuka- neocaledoniensis, niigatensis, ninae, nova, polyresistens, pseudobrasil- murella paurometabola and the closely related species Tsukamurella iensis, pseudovaccinii, seriolae, takedensis, tenerifensis, terpenica, thai- carboxydivorans, inchonensis, pseudospumae, pulmonis, spongiae, spu- landica, transvalensis, uniformis, vinacea, wallacei, xishanensis, and mae, strandjordii, sunchonensis, and tyrosinosolvens. The presence yamanashiensis. This cluster also contains three subclades that of a completely unsaturated menaquinone MK-9 detected in all are well differentiated from the other species: Nocardia brevicat- species of this group supports placement in a single genus. ena and paucivorans; Nocardia carnea, flavorosea, jinanensis, pig- Order “Frankiales” rifrangens, sienata, speluncae, and testacea; and Nocardia coubleae, cummidelens, fluminea, ignorata, salmonicida, and soli. The second This order is formed by elevation of the suborder of Frankineae cluster includes Nocardia africana, amamiensis, aobensis, araoensis, (Stackebrandt et al., 1997; Zhi et al., 2009) and comprises the arthritidis, beijingensis, cerradoensis, elegans, kruczakiae, pneumoniae, families Frankiaceae, Acidothermaceae, Cryptosporangiaceae, Geoder- vaccinii, vermiculata, and veterana. The third cluster is at the base matophilaceae, Nakamurellaceae, and Sporichthyaceae (Figure 7). of the Nocardia lineage and includes the species Nocardia asiat- The major difference between this order and the correspond- ica, farcinica, higoensis, otitidiscaviarum, puris, and shimofusensis. ing group described in the previous road map (Garrity et al., The genus Gordonia is represented by a well-defined clade 2005) is the reclassification of the genera Kineosporia and Kine- comprising the type species Gordonia bronchialis and Gordonia ococcus to the novel order “Kineosporiales” (Zhi et al., 2009). In aichiensis, alkanivorans, amarae, amicalis, araii, cholesterolivorans, addition, the family Cryptosporangiaceae was proposed to include defluvii, desulfuricans, effusa, hankookensis, hirsuta, hydrophobica, the genus Cryptosporangium, which had previously been classi- kroppenstedtii, lacunae, malaquae, namibiensis, otitidis, paraffiniv- fied within the family Kineosporiaceae but was retained in the orans, polyisoprenivorans, rhizosphera, rubripertincta, shandongensis, “Frankiales”. Lastly, the previous road map included the mono- sihwensis, sinesedis, soli, sputi, terrae, and westfalica. It is closely generic family Microsphaeraceae. However, this genus name was related to the genus Williamsia, a relationship that is also sup- ruled illegitimate because of precedence of a fungal genus, and ported by similarities in menaquinone content and other the bacterial species was reclassified to the new family Naka- chemotaxonomic markers (Goodfellow and Jones, 2012). murellaceae (Tao et al., 2004). In the rRNA gene tree, the monospecific genus Millisia (type Although the group “Frankiales” was observed in early stud- species Millisia brevis) is related to the genera Gordonia and Wil- ies of the phylogeny of the 16S rRNA gene in Actinobacteria liamsia. This relationship is also consistent with similarities in (Normand et al., 1996; Stackebrandt et al., 1997), more recent the chain lengths of their mycolic acids. studies with different selections of outgroups and other meth- The genus Rhodococcus is represented by a number of deep, ods of phylogenetic analyses do not provide strong support for paraphyletic lineages with short branch lengths at the base this classification. For instance, although 16S rRNA gene sig- of the radiation including the family Nocardiaceae and order natures have been proposed for the order, there is little boot- “Corynebacteriales”. One clade comprises the type species Rho- strap support for this group in the 16S rRNA gene tree of Zhi dococcus rhodochrous and Rhodococcus aetherivorans, coprophilus, et al. (2009). In the gene trees prepared for this volume, only gordoniae, phenolicus, pyridinivorans, ruber, and zopfii. A second, the families Frankiaceae and Acidothermaceae are closely related poorly resolved clade encompasses Rhodococcus baikonurensis, (Figures 2 and 7), a relationship also observed by Zhi et al. 8 ROAD MAP

growth distinguish this moderately thermophilic taxon from the Frankiaceae.

"Streptosporangiales" Family Cryptosporangiaceae This family comprises the genus Cryptosporangium. It contains the type species Cryptosporangium arvum and three closely Blastococcus related species Cryptosporangium aurantiacum, japonicum, and minutisporangium. Based upon similarities in its 16S rRNA gene Geodermatophilaceae Modestobacter sequence, the monospecific genus Fodinicola (type species Fodinicola feengrottensis) is tentatively classified in this family as Geodermatophilus a genus incertae sedis.

Sporichthya − Sporichthyaceae Family Geodermatophilaceae The type for this family is the monospecific genus Geodermato- Humicoccus philus (type species Geodermatophilus obscurus). Other gen- Saxeibacter Nakamurellaceae era and species include Blastococcus aggregatus (type species), Nakamurella jejuensis, and saxobsidens, as well as Modestobacter multiseptatus (type species) and versicolor. Cryptosporangium Cryptosporangiaceae Family Nakamurellaceae Fodinicola This family comprises three monospecific genera: Nakamurella Acidothermus − Acidothermaceae (type species Nakamurella multipartita), Humicoccus (type species Humicoccus flavidus), and Saxeibacter (type species Saxeibacter Frankia − Frankiaceae lacteus). This latter is a recently described genus which is not described further in this volume (Lee et al., 2008). FIGURE 7. Genera and families of the order “Frankiales”. Analyses were performed as described for Figure 1. Family Sporichthyaceae This monogeneric family encompasses two closely related (2009) and supported by similarities in recA genes (Marechal species: Sporichthya polymorpha (type species) and Sporichthya et al., 2000). The remaining families appear as deep lineages of brevicatena. the class Actinobacteria but are not specifically related to the fam- ily Frankiaceae. Chemotaxonomic evidence does not fully resolve Order “Glycomycetales” and family Glycomycetaceae this issue (Normand and Benson, 2012). The cell-wall diamino This order is formed by elevation of the suborder Glycomy- acid is meso-diaminopimelate in all families tested except for the cineae (Stackebrandt et al., 1997; Zhi et al., 2009) and com- family Sporichthyaceae, which contains ll-diaminopimelate. In prises the single family Glycomycetaceae. In the 16S rRNA gene the families Frankiaceae, Cryptosporangiaceae, and Sporichthyaceae, trees prepared for this volume, the “Glycomycetales” appears as the abundant menaquinones are MK-9(H4), MK-9(H6), and a long branch specifically related to the genus Actinocatenispora

MK-9(H8). However, Geodermatophilaceae contains MK-9(H4) within the order “Micromonosporales” (Figure 8). Some chemot- and MK-8(H4); and Nakamurellaceae contains mostly MK-8(H4). axonomic and phenotypic properties tend to support this asso- The menaquinones of the Acidothermaceae have not been deter- ciation (Labeda, 2012; Matsumoto et al., 2007; Seo and Lee, mined. Lastly, the fatty acid composition is also diverse. Mem- 2009; Thawai et al., 2006). The family Glycomycetaceae and Acti- bers of all families contain mostly saturated fatty acids in the nocatenispora each have type II cell walls which contain meso- range of 15–18 carbons, some or all of which are branched. diaminopimelic acid and glycine as well as N-glycolylmuramic Thus, while the chemotaxonomic evidence identifies some uni- acid. They also produce chains of spores on aerial hyphae. fying features, it does not provide strong evidence for the order However, some differences also exist. Glycomycetaceae and Acti- “Frankiales”. Hence, its composition should be considered ten- nocatenispora possess phospholipid types I and II, respectively. tative until conclusive evidence is available. Moreover, in the Glycomycetaceae, MK-10, MK-11, and MK-12 menaquinones are abundant, whereas in the Actinocatenispora, Family Frankiaceae MK-9 (H4, H6) menaquinones predominate. For these reasons, This monogeneric family comprises the type genus Frankia the association between these two taxa is considered tentative (type and only species Frankia alni). Common nitrogen-fixing at this time. symbionts of dicotyledonous plants, at least 12 genospecies The family Glycomycetaceae contains three genera. The genus have been isolated but their names have not been validly pub- Glycomyces encompasses the type species Glycomyces harbinensis lished. Hence, the diversity of the genus is certainly larger than and nine other species: Glycomyces algeriensis, arizonensis, endo- represented by the nomenclature. phyticus, lechevalierae, mayteni, rutgersensis, sambucus, scopariae, and tenuis. Closely related is the recently described monospe- Family Acidothermaceae cific genus Haloglycomyces (type species Haloglycomyces albus), This monogeneric family comprises the type genus Acidother- which is not described in this volume (Guan et al., 2009). Lastly, mus (type and only species Acidothermus cellulolyticus). Its growth the genus Stackebrandtia contains the type species Stackebrandtia temperature range of 37–70°C, inability to fix N2, and rapid nassauensis and Stackebrandtia albiflava. ROAD MAP 9

Jiangela Jiangellaceae − "Jiangellales" Haloactinopolyspora

Micromonospora

Planosporangium

Catellatospora

Dactylosporangium

Virgisporangium

Luedemannella

Rugosimonospora

Plantactinospora

Actinoplanes

Micromonosporaceae Catenuloplanes "Micromonosporales"

Verrucosispora

Hamadaea

Catelliglobosispora

Asanoa

Spirilliplanes

Salinispora

Krasilnikovia Pseudosporangium Couchioplanes Longispora Polymorphospora

Pilimelia

Actinocatenispora

Glycomyces Glycomycetaceae Haloglycomyces "Glycomycetales"

Stackebrandtia

FIGURE 8. Genera of the orders “Glycomycetales”, “Jiangellales”, and “Micromonosporales”. Analyses were performed as described for Figure 1.