DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Paraburkholderia solitsugae sp. nov. and Paraburkholderia elongata sp. nov., phenolic acid-degrading bacteria isolated from forest soil and emended description of Paraburkholderia madseniana

Abstract

Two bacterial strains, 1NT and 5NT, were isolated from hemlock forest soil using a soluble organic matter enrichment. Cells of 1NT (0.65×1.85 µm) and 5NT (0.6×1.85 µm) are Gram-stain-negative, aerobic, motile, non-sporulating and exist as single rods, diplobacilli or in chains of varying length. During growth in dilute media (≤0.1× tryptic soy broth; TSB), cells are primarily motile with flagella. At higher concentrations (≥0.3× TSB), cells of both strains increasingly form non-motile chains, and cells of 5NT elongate (0.57×~7 µm) and form especially long filaments. Optimum growth of 1NT and 5NT occurred at 25–30 °C, pH 6.5–7.0 and <0.5% salinity. Results of comparative chemotaxonomic, genomic and phylogenetic analyses revealed that 1NT and 5NT were distinct from one another and their closest related type strains: Paraburkholderia madseniana RP11T, Paraburkholderia aspalathi LMG 27731T and Paraburkholderia caffeinilytica CF1T. The genomes of 1NT and 5NT had an average nucleotide identity (91.6 and 91.3%) and in silico DNA–DNA hybridization values (45.8%±2.6 and 45.5%±2.5) and differed in functional gene content from their closest related type strains. The composition of fatty acids and patterns of substrate use, including the catabolism of phenolic acids, also differentiated strains 1NT and 5NT from each other and their closest relatives. Themore » only ubiquinone present in strains 1NT and 5NT was Q-8. The major cellular fatty acids were C16 : 0, 3OH-C16 : 0, C17 : 0 cyclo, C19 : 0 cyclo ω8c and summed features 2 (3OH-C14 : 0 / C16 : 1 iso I), 3 (C16 : 1 ω6c/ω7c) and 8 (C18 : 1 ω7c/ω6c). A third bacterium, strain RL16-012-BIC-B, was isolated from soil associated with shallow roots and was determined to be a strain of P. madseniana (ANI, 98.8%; 16S rRNA gene similarity, 100%). Characterizations of strain RL16-012-BIC-B (DSM 110723=LMG 31706) led to proposed emendments to the species description of P. madseniana . Here, our polyphasic approach demonstrated that strains 1NT and 5NT represent novel species from the genus Paraburkholderia for which the names Paraburkholderia solitsugae sp. nov. (type strain 1NT=DSM 110721T=LMG 31704T) and Paraburkholderia elongata sp. nov. (type strain 5NT=DSM 110722T=LMG 31705T) are proposed.« less

Authors:
 [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]
  1. Cornell Univ., Ithaca, NY (United States)
  2. Lycoming College, Williamsport, PA (United States)
Publication Date:
Research Org.:
Cornell Univ., Ithaca, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science (BSS)
OSTI Identifier:
1863906
Alternate Identifier(s):
OSTI ID: 2228925
Grant/Contract Number:  
SC0016364
Resource Type:
Accepted Manuscript
Journal Name:
International Journal of Systematic and Evolutionary Microbiology
Additional Journal Information:
Journal Volume: 70; Journal Issue: 9; Journal ID: ISSN 1466-5026
Publisher:
International Union of Microbiological Societies
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Wilhelm, Roland C., Cyle, K. Taylor, Martinez, Carmen Enid, Karasz, David C., Newman, Jeffrey D., and Buckley, Daniel H. Paraburkholderia solitsugae sp. nov. and Paraburkholderia elongata sp. nov., phenolic acid-degrading bacteria isolated from forest soil and emended description of Paraburkholderia madseniana. United States: N. p., 2020. Web. doi:10.1099/ijsem.0.004387.
Wilhelm, Roland C., Cyle, K. Taylor, Martinez, Carmen Enid, Karasz, David C., Newman, Jeffrey D., & Buckley, Daniel H. Paraburkholderia solitsugae sp. nov. and Paraburkholderia elongata sp. nov., phenolic acid-degrading bacteria isolated from forest soil and emended description of Paraburkholderia madseniana. United States. https://doi.org/10.1099/ijsem.0.004387
Wilhelm, Roland C., Cyle, K. Taylor, Martinez, Carmen Enid, Karasz, David C., Newman, Jeffrey D., and Buckley, Daniel H. Tue . "Paraburkholderia solitsugae sp. nov. and Paraburkholderia elongata sp. nov., phenolic acid-degrading bacteria isolated from forest soil and emended description of Paraburkholderia madseniana". United States. https://doi.org/10.1099/ijsem.0.004387. https://www.osti.gov/servlets/purl/1863906.
@article{osti_1863906,
title = {Paraburkholderia solitsugae sp. nov. and Paraburkholderia elongata sp. nov., phenolic acid-degrading bacteria isolated from forest soil and emended description of Paraburkholderia madseniana},
author = {Wilhelm, Roland C. and Cyle, K. Taylor and Martinez, Carmen Enid and Karasz, David C. and Newman, Jeffrey D. and Buckley, Daniel H.},
abstractNote = {Two bacterial strains, 1NT and 5NT, were isolated from hemlock forest soil using a soluble organic matter enrichment. Cells of 1NT (0.65×1.85 µm) and 5NT (0.6×1.85 µm) are Gram-stain-negative, aerobic, motile, non-sporulating and exist as single rods, diplobacilli or in chains of varying length. During growth in dilute media (≤0.1× tryptic soy broth; TSB), cells are primarily motile with flagella. At higher concentrations (≥0.3× TSB), cells of both strains increasingly form non-motile chains, and cells of 5NT elongate (0.57×~7 µm) and form especially long filaments. Optimum growth of 1NT and 5NT occurred at 25–30 °C, pH 6.5–7.0 and <0.5% salinity. Results of comparative chemotaxonomic, genomic and phylogenetic analyses revealed that 1NT and 5NT were distinct from one another and their closest related type strains: Paraburkholderia madseniana RP11T, Paraburkholderia aspalathi LMG 27731T and Paraburkholderia caffeinilytica CF1T. The genomes of 1NT and 5NT had an average nucleotide identity (91.6 and 91.3%) and in silico DNA–DNA hybridization values (45.8%±2.6 and 45.5%±2.5) and differed in functional gene content from their closest related type strains. The composition of fatty acids and patterns of substrate use, including the catabolism of phenolic acids, also differentiated strains 1NT and 5NT from each other and their closest relatives. The only ubiquinone present in strains 1NT and 5NT was Q-8. The major cellular fatty acids were C16 : 0, 3OH-C16 : 0, C17 : 0 cyclo, C19 : 0 cyclo ω8c and summed features 2 (3OH-C14 : 0 / C16 : 1 iso I), 3 (C16 : 1 ω6c/ω7c) and 8 (C18 : 1 ω7c/ω6c). A third bacterium, strain RL16-012-BIC-B, was isolated from soil associated with shallow roots and was determined to be a strain of P. madseniana (ANI, 98.8%; 16S rRNA gene similarity, 100%). Characterizations of strain RL16-012-BIC-B (DSM 110723=LMG 31706) led to proposed emendments to the species description of P. madseniana . Here, our polyphasic approach demonstrated that strains 1NT and 5NT represent novel species from the genus Paraburkholderia for which the names Paraburkholderia solitsugae sp. nov. (type strain 1NT=DSM 110721T=LMG 31704T) and Paraburkholderia elongata sp. nov. (type strain 5NT=DSM 110722T=LMG 31705T) are proposed.},
doi = {10.1099/ijsem.0.004387},
journal = {International Journal of Systematic and Evolutionary Microbiology},
number = 9,
volume = 70,
place = {United States},
year = {Tue Aug 18 00:00:00 EDT 2020},
month = {Tue Aug 18 00:00:00 EDT 2020}
}

Works referenced in this record:

Burkholderia symbiotica sp. nov., isolated from root nodules of Mimosa spp. native to north-east Brazil
journal, November 2011

  • Sheu, S. -Y.; Chou, J. -H.; Bontemps, C.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 62, Issue Pt 9
  • DOI: 10.1099/ijs.0.037408-0

LC–MS method for screening unknown microbial carotenoids and isoprenoid quinones
journal, January 2012


Prevalent root-derived phenolics drive shifts in microbial community composition and prime decomposition in forest soil
journal, June 2020


MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms
journal, May 2018

  • Kumar, Sudhir; Stecher, Glen; Li, Michael
  • Molecular Biology and Evolution, Vol. 35, Issue 6
  • DOI: 10.1093/molbev/msy096

Burkholderia dilworthii sp. nov., isolated from Lebeckia ambigua root nodules
journal, December 2013

  • De Meyer, S. E.; Cnockaert, M.; Ardley, J. K.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 4
  • DOI: 10.1099/ijs.0.058602-0

Burkholderia humi sp. nov., Burkholderia choica sp. nov., Burkholderia telluris sp. nov., Burkholderia terrestris sp. nov. and Burkholderia udeis sp. nov.: Burkholderia glathei-like bacteria from soil and rhizosphere soil
journal, December 2013

  • Vandamme, Peter; De Brandt, Evie; Houf, Kurt
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 63, Issue Pt_12
  • DOI: 10.1099/ijs.0.048900-0

Complete Genome Sequence of the Plant Growth-Promoting Endophyte Burkholderia phytofirmans Strain PsJN
journal, May 2011

  • Weilharter, A.; Mitter, B.; Shin, M. V.
  • Journal of Bacteriology, Vol. 193, Issue 13
  • DOI: 10.1128/JB.05055-11

Burkholderia caballeronis sp. nov., a nitrogen fixing species isolated from tomato (Lycopersicon esculentum) with the ability to effectively nodulate Phaseolus vulgaris
journal, September 2013

  • Martínez-Aguilar, Lourdes; Salazar-Salazar, Corelly; Méndez, Rafael Díaz
  • Antonie van Leeuwenhoek, Vol. 104, Issue 6
  • DOI: 10.1007/s10482-013-0028-9

Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014


Burkholderia rhizoxinica sp. nov. and Burkholderia endofungorum sp. nov., bacterial endosymbionts of the plant-pathogenic fungus Rhizopus microsporus
journal, November 2007

  • Partida-Martinez, L. P.; Groth, I.; Schmitt, I.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 11
  • DOI: 10.1099/ijs.0.64660-0

Burkholderia nodosa sp. nov., isolated from root nodules of the woody Brazilian legumes Mimosa bimucronata and Mimosa scabrella
journal, May 2007

  • Chen, W. -M.; de Faria, S. M.; James, E. K.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 5
  • DOI: 10.1099/ijs.0.64873-0

Indole-3-Acetic Acid in Burkholderia pyrrocinia JK-SH007: Enzymatic Identification of the Indole-3-Acetamide Synthesis Pathway
journal, November 2019


Genome Data Provides High Support for Generic Boundaries in Burkholderia Sensu Lato
journal, June 2017

  • Beukes, Chrizelle W.; Palmer, Marike; Manyaka, Puseletso
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.01154

Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp. and fixes nitrogen ex planta
journal, October 2006


Utilization of simple phenolics for dinitrogen fixation by soil diazotrophic bacteria
journal, February 1986


BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs
journal, June 2015


Rapid Method for Coextraction of DNA and RNA from Natural Environments for Analysis of Ribosomal DNA- and rRNA-Based Microbial Community Composition
journal, December 2000


FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


SignalP 5.0 improves signal peptide predictions using deep neural networks
journal, February 2019

  • Almagro Armenteros, José Juan; Tsirigos, Konstantinos D.; Sønderby, Casper Kaae
  • Nature Biotechnology, Vol. 37, Issue 4
  • DOI: 10.1038/s41587-019-0036-z

Soil processes drive seasonal variation in retention of 15 N tracers in a deciduous forest catchment
journal, October 2015

  • Goodale, Christine L.; Fredriksen, Guinevere; Weiss, Marissa S.
  • Ecology, Vol. 96, Issue 10
  • DOI: 10.1890/14-1852.1

Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium
journal, November 2004

  • Reis, V. M.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 6
  • DOI: 10.1099/ijs.0.02879-0

Draft genome sequence of Paraburkholderia tropica Ppe8 strain, a sugarcane endophytic diazotrophic bacterium
journal, April 2018

  • Silva, Paula Renata Alves da; Simões-Araújo, Jean Luiz; Vidal, Márcia Soares
  • Brazilian Journal of Microbiology, Vol. 49, Issue 2
  • DOI: 10.1016/j.bjm.2017.07.005

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


Quorum Sensing and Indole-3-Acetic Acid Degradation Play a Role in Colonization and Plant Growth Promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN
journal, May 2013

  • Zúñiga, Ana; Poupin, María Josefina; Donoso, Raúl
  • Molecular Plant-Microbe Interactions, Vol. 26, Issue 5
  • DOI: 10.1094/MPMI-10-12-0241-R

Taxonomic use of DNA G+C content and DNA–DNA hybridization in the genomic age
journal, February 2014

  • Klenk, Hans-Peter; Meier-Kolthoff, Jan P.; Göker, Markus
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 64, Issue 2
  • DOI: 10.1099/ijs.0.056994-0

Integrative genomics viewer
journal, January 2011

  • Robinson, James T.; Thorvaldsdóttir, Helga; Winckler, Wendy
  • Nature Biotechnology, Vol. 29, Issue 1
  • DOI: 10.1038/nbt.1754

Burkholderia bannensis sp. nov., an acid-neutralizing bacterium isolated from torpedo grass (Panicum repens) growing in highly acidic swamps
journal, July 2011

  • Aizawa, Tomoko; Vijarnsorn, Pisoot; Nakajima, Mutsuyasu
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 61, Issue 7
  • DOI: 10.1099/ijs.0.026278-0

Burkholderia sprentiae sp. nov., isolated from Lebeckia ambigua root nodules
journal, May 2013

  • De Meyer, S. E.; Cnockaert, M.; Ardley, J. K.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 11
  • DOI: 10.1099/ijs.0.048777-0

Burkholderia mimosarum sp. nov., isolated from root nodules of Mimosa spp. from Taiwan and South America
journal, August 2006

  • Chen, W. -M.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 8
  • DOI: 10.1099/ijs.0.64325-0

Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., Nodulate the Roots of Tropical Legumes
journal, January 2002

  • Vandamme, Peter; Goris, Johan; Chen, Wen-Ming
  • Systematic and Applied Microbiology, Vol. 25, Issue 4
  • DOI: 10.1078/07232020260517634

NIH Image to ImageJ: 25 years of image analysis
journal, June 2012

  • Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2089

A Third Class: Functional Gibberellin Biosynthetic Operon in Beta-Proteobacteria
journal, November 2018

  • Nagel, Raimund; Bieber, John E.; Schmidt-Dannert, Mark G.
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.02916

Burkholderia aspalathi sp. nov., isolated from root nodules of the South African legume Aspalathus abietina Thunb
journal, March 2014

  • Mavengere, N. R.; Ellis, A. G.; Le Roux, J. J.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 6
  • DOI: 10.1099/ijs.0.057067-0

Burkholderia unamae sp. nov., an N2-fixing rhizospheric and endophytic species
journal, July 2004

  • Caballero-Mellado, Jesús; Martínez-Aguilar, Lourdes; Paredes-Valdez, Guadalupe
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 54, Issue 4
  • DOI: 10.1099/ijs.0.02951-0

A selective genome-guided method for environmental Burkholderia isolation
journal, January 2019

  • Haeckl, F. P. Jake; Baldim, João L.; Iskakova, Dasha
  • Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 3-4
  • DOI: 10.1007/s10295-018-02121-x

KBase: The United States Department of Energy Systems Biology Knowledgebase
journal, July 2018

  • Arkin, Adam P.; Cottingham, Robert W.; Henry, Christopher S.
  • Nature Biotechnology, Vol. 36, Issue 7
  • DOI: 10.1038/nbt.4163

Burkholderia sediminicola sp. nov., isolated from freshwater sediment
journal, March 2008

  • Lim, J. H.; Baek, S. -H.; Lee, S. -T.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 58, Issue 3
  • DOI: 10.1099/ijs.0.65502-0

SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012

  • Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
  • Journal of Computational Biology, Vol. 19, Issue 5
  • DOI: 10.1089/cmb.2012.0021

Burkholderia diazotrophica sp. nov., isolated from root nodules of Mimosa spp.
journal, March 2012

  • Sheu, S. -Y.; Chou, J. -H.; Bontemps, C.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 2
  • DOI: 10.1099/ijs.0.039859-0

Role and Regulation of ACC Deaminase Gene in Sinorhizobium meliloti: Is It a Symbiotic, Rhizospheric or Endophytic Gene?
journal, January 2017


Transfer of eleven species of the genus Burkholderia to the genus Paraburkholderia and proposal of Caballeronia gen. nov. to accommodate twelve species of the genera Burkholderia and Paraburkholderia
journal, August 2016

  • Dobritsa, Anatoly P.; Samadpour, Mansour
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 8
  • DOI: 10.1099/ijsem.0.001065

Paraburkholderia phosphatilytica sp. nov., a phosphate-solubilizing bacterium isolated from forest soil
journal, January 2019

  • Gao, Zeng-hong; Ruan, Shao-lin; Huang, Yi-xian
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 69, Issue 1
  • DOI: 10.1099/ijsem.0.003129

High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries
journal, November 2018


Complete Genome Sequence of Burkholderia phenoliruptrix BR3459a (CLA1), a Heat-Tolerant, Nitrogen-Fixing Symbiont of Mimosa flocculosa
journal, November 2012

  • de Oliveira Cunha, Cláudio; Goda Zuleta, Luiz Fernando; Paula de Almeida, Luiz Gonzaga
  • Journal of Bacteriology, Vol. 194, Issue 23
  • DOI: 10.1128/JB.01821-12

Halomonas elongata, a New Genus and Species of Extremely Salt-Tolerant Bacteria
journal, April 1980

  • Vreeland, R. H.; Litchfield, C. D.; Martin, E. L.
  • International Journal of Systematic Bacteriology, Vol. 30, Issue 2
  • DOI: 10.1099/00207713-30-2-485

Burkholderia silvatlantica sp. nov., a diazotrophic bacterium associated with sugar cane and maize
journal, August 2006

  • Perin, L.; Martínez-Aguilar, L.; Paredes-Valdez, G.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 56, Issue 8
  • DOI: 10.1099/ijs.0.64362-0

The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST)
journal, November 2013

  • Overbeek, Ross; Olson, Robert; Pusch, Gordon D.
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1226

Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing
journal, September 2018


Transport of Carbon and Nitrogen Between Litter and Soil Organic Matter in a Northern Hardwood Forest
journal, February 2011


Profile hidden Markov models
journal, October 1998


MicrobeJ, a tool for high throughput bacterial cell detection and quantitative analysis
journal, June 2016


Symbiotic and non-symbiotic Paraburkholderia isolated from South African Lebeckia ambigua root nodules and the description of Paraburkholderia fynbosensis sp. nov.
journal, August 2018

  • De Meyer, Sofie E.; Cnockaert, Margo; Moulin, Lionel
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 68, Issue 8
  • DOI: 10.1099/ijsem.0.002884

DNA–DNA hybridization values and their relationship to whole-genome sequence similarities
journal, January 2007

  • Klappenbach, Joel A.; Goris, Johan; Vandamme, Peter
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 1
  • DOI: 10.1099/ijs.0.64483-0

Ragout--a reference-assisted assembly tool for bacterial genomes
journal, June 2014