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Title: Phylogenomic Insight into Salinispora (Bacteria, Actinobacteria) Species Designations

Abstract

Bacteria represent the most genetically diverse kingdom of life. While great progress has been made in describing this diversity, it remains difficult to identify the phylogenetic and ecological characteristics that delineate groups of bacteria that possess species-like properties. One major challenge associated with species delineations is that not all shared genes have the same evolutionary history, and thus the choice of loci can have a major impact on phylogenetic reconstruction. Sequencing the genomes of large numbers of closely related strains provides new opportunities to distinguish ancestral from acquired alleles and assess the effects of recombination on phylogenetic inference. Here we analyzed the genomes of 119 strains of the marine actinomycete genus Salinispora, which is currently comprised of three named species that share 99% 16S rRNA gene sequence identity. While 63% of the core genome showed evidence of recombination, this had no effect on species-level phylogenomic resolution. Recombination did however blur intra-species relationships and biogeographic resolution. The genome-wide average nucleotide identity provided a new perspective on Salinispora diversity, revealing as many as seven new species. Patterns of orthologous group distributions reveal a genetic basis to delineation the candidate taxa and insight into the levels of genetic cohesion associated with bacterial species.

Authors:
 [1];  [2];  [3];  [2];  [2];  [2]
  1. Univ. of California, San Diego, CA (United States). Scripps Inst. of Oceanography; Universidad Autónoma de Baja California., Ensenada, Baja California (Mexico)
  2. Univ. of California, San Diego, CA (United States). Scripps Inst. of Oceanography
  3. Univ. of California, San Diego, CA (United States). Scripps Inst. of Oceanography; Univ. Andrés Bella, Santiago, (Chile)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF); National Institutes of Health (NIH); Amazon Web Services; Consejo Nacional de Ciencia y Tecnología; FCT/MEC
OSTI Identifier:
1624295
Grant/Contract Number:  
AC02-05CH11231; OCE-1235142; 2U19TW007401; 5R01GM085770; Fondecyt Iniciación 11140666; CONACyT-213497; PTDC/QUI-QUI/119116/2010; IF/00700/2014
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; science & technology; bacterial genomics; microbiology

Citation Formats

Millán-Aguiñaga, Natalie, Chavarria, Krystle L., Ugalde, Juan A., Letzel, Anne-Catrin, Rouse, Greg W., and Jensen, Paul R. Phylogenomic Insight into Salinispora (Bacteria, Actinobacteria) Species Designations. United States: N. p., 2017. Web. doi:10.1038/s41598-017-02845-3.
Millán-Aguiñaga, Natalie, Chavarria, Krystle L., Ugalde, Juan A., Letzel, Anne-Catrin, Rouse, Greg W., & Jensen, Paul R. Phylogenomic Insight into Salinispora (Bacteria, Actinobacteria) Species Designations. United States. https://doi.org/10.1038/s41598-017-02845-3
Millán-Aguiñaga, Natalie, Chavarria, Krystle L., Ugalde, Juan A., Letzel, Anne-Catrin, Rouse, Greg W., and Jensen, Paul R. Thu . "Phylogenomic Insight into Salinispora (Bacteria, Actinobacteria) Species Designations". United States. https://doi.org/10.1038/s41598-017-02845-3. https://www.osti.gov/servlets/purl/1624295.
@article{osti_1624295,
title = {Phylogenomic Insight into Salinispora (Bacteria, Actinobacteria) Species Designations},
author = {Millán-Aguiñaga, Natalie and Chavarria, Krystle L. and Ugalde, Juan A. and Letzel, Anne-Catrin and Rouse, Greg W. and Jensen, Paul R.},
abstractNote = {Bacteria represent the most genetically diverse kingdom of life. While great progress has been made in describing this diversity, it remains difficult to identify the phylogenetic and ecological characteristics that delineate groups of bacteria that possess species-like properties. One major challenge associated with species delineations is that not all shared genes have the same evolutionary history, and thus the choice of loci can have a major impact on phylogenetic reconstruction. Sequencing the genomes of large numbers of closely related strains provides new opportunities to distinguish ancestral from acquired alleles and assess the effects of recombination on phylogenetic inference. Here we analyzed the genomes of 119 strains of the marine actinomycete genus Salinispora, which is currently comprised of three named species that share 99% 16S rRNA gene sequence identity. While 63% of the core genome showed evidence of recombination, this had no effect on species-level phylogenomic resolution. Recombination did however blur intra-species relationships and biogeographic resolution. The genome-wide average nucleotide identity provided a new perspective on Salinispora diversity, revealing as many as seven new species. Patterns of orthologous group distributions reveal a genetic basis to delineation the candidate taxa and insight into the levels of genetic cohesion associated with bacterial species.},
doi = {10.1038/s41598-017-02845-3},
journal = {Scientific Reports},
number = 1,
volume = 7,
place = {United States},
year = {Thu Jun 15 00:00:00 EDT 2017},
month = {Thu Jun 15 00:00:00 EDT 2017}
}

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Works referenced in this record:

Comparative and Evolutionary Analysis of the Bacterial Homologous Recombination Systems
journal, January 2005


Comparative and Evolutionary Analysis of the Bacterial Homologous Recombination Systems
journal, January 2005


Microdiversity and evidence for high dispersal rates in the marine actinomycete ‘Salinispora pacifica’: Salinispora microdiversity
journal, November 2011


Identification of Thiotetronic Acid Antibiotic Biosynthetic Pathways by Target-directed Genome Mining
journal, October 2015


Microbial taxonomy in the post-genomic era: Rebuilding from scratch?
journal, December 2014

  • Thompson, Cristiane C.; Amaral, Gilda R.; Campeão, Mariana
  • Archives of Microbiology, Vol. 197, Issue 3
  • DOI: 10.1007/s00203-014-1071-2

OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
journal, September 2003


Genomic basis for natural product biosynthetic diversity in the actinomycetes
journal, January 2009

  • Nett, Markus; Ikeda, Haruo; Moore, Bradley S.
  • Natural Product Reports, Vol. 26, Issue 11
  • DOI: 10.1039/b817069j

The marine actinomycete genus Salinispora: a model organism for secondary metabolite discovery
journal, January 2015

  • Jensen, Paul R.; Moore, Bradley S.; Fenical, William
  • Natural Product Reports, Vol. 32, Issue 5
  • DOI: 10.1039/c4np00167b

RNA polymerase II stalling: loading at the start prepares genes for a sprint
journal, January 2008


Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species
journal, October 2010


DNA Sequence Similarity Requirements for Interspecific Recombination in Bacillus
journal, December 1999


Salinispora pacifica sp. nov., an actinomycete from marine sediments
journal, January 2013


Identification of Thiotetronic Acid Antibiotic Biosynthetic Pathways by Target-directed Genome Mining
journal, October 2015


Contributions of ancestral inter-species recombination to the genetic diversity of extant Streptomyces lineages
journal, February 2016

  • Andam, Cheryl P.; Choudoir, Mallory J.; Vinh Nguyen, Anh
  • The ISME Journal, Vol. 10, Issue 7
  • DOI: 10.1038/ismej.2015.230

Diversity and evolution of secondary metabolism in the marine actinomycete genus Salinispora
journal, March 2014

  • Ziemert, N.; Lechner, A.; Wietz, M.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 12
  • DOI: 10.1073/pnas.1324161111

Microdiversity and evidence for high dispersal rates in the marine actinomycete ‘Salinispora pacifica’: Salinispora microdiversity
journal, November 2011


Bacterial Self-Resistance to the Natural Proteasome Inhibitor Salinosporamide A
journal, September 2011

  • Kale, Andrew J.; McGlinchey, Ryan P.; Lechner, Anna
  • ACS Chemical Biology, Vol. 6, Issue 11
  • DOI: 10.1021/cb2002544

A Simple and Robust Statistical Test for Detecting the Presence of Recombination
journal, February 2006


Bacterial Self-Resistance to the Natural Proteasome Inhibitor Salinosporamide A
journal, September 2011

  • Kale, Andrew J.; McGlinchey, Ryan P.; Lechner, Anna
  • ACS Chemical Biology, Vol. 6, Issue 11
  • DOI: 10.1021/cb2002544

A Simple and Robust Statistical Test for Detecting the Presence of Recombination
journal, February 2006


Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology.
journal, May 2002

  • Garrity, George M.; Trüper, Hans G.; Whitman, William B.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 52, Issue 3
  • DOI: 10.1099/00207713-52-3-1043

ASTRAL: genome-scale coalescent-based species tree estimation
journal, August 2014


Widespread homologous recombination within and between Streptomyces species
journal, April 2010


Widespread homologous recombination within and between Streptomyces species
journal, April 2010


Comparison of 61 Sequenced Escherichia coli Genomes
journal, July 2010

  • Lukjancenko, Oksana; Wassenaar, Trudy M.; Ussery, David W.
  • Microbial Ecology, Vol. 60, Issue 4
  • DOI: 10.1007/s00248-010-9717-3

Salinispora arenicola gen. nov., sp. nov. and Salinispora tropica sp. nov., obligate marine actinomycetes belonging to the family Micromonosporaceae
journal, September 2005

  • Maldonado, L. A.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 55, Issue 5
  • DOI: 10.1099/ijs.0.63625-0

Adaptation of Hansenula polymorpha to methanol: a transcriptome analysis
journal, January 2010

  • van Zutphen, Tim; Baerends, Richard JS; Susanna, Kim A.
  • BMC Genomics, Vol. 11, Issue 1
  • DOI: 10.1186/1471-2164-11-1

The Bacterial Species Challenge: Making Sense of Genetic and Ecological Diversity
journal, February 2009


Re-evaluating prokaryotic species
journal, August 2005

  • Gevers, Dirk; Cohan, Frederick M.; Lawrence, Jeffrey G.
  • Nature Reviews Microbiology, Vol. 3, Issue 9
  • DOI: 10.1038/nrmicro1236

Recombination and the Nature of Bacterial Speciation
journal, January 2007


Diversity and distribution of the bioactive actinobacterial genus Salinispora from sponges along the Great Barrier Reef
journal, November 2011


Phylogenomics: Improving Functional Predictions for Uncharacterized Genes by Evolutionary Analysis
journal, March 1998


RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006


Barriers to Genetic Exchange between Bacterial Species: Streptococcus pneumoniae Transformation
journal, February 2000


Inconsistency of Phylogenetic Estimates from Concatenated Data under Coalescence
journal, February 2007


Genomes of diverse isolates of the marine cyanobacterium Prochlorococcus
journal, September 2014

  • Biller, Steven J.; Berube, Paul M.; Berta-Thompson, Jessie W.
  • Scientific Data, Vol. 1, Issue 1
  • DOI: 10.1038/sdata.2014.34

RDP3: a flexible and fast computer program for analyzing recombination
journal, August 2010


OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
journal, September 2003


Sequences, sequence clusters and bacterial species
journal, October 2006

  • Hanage, William P.; Fraser, Christophe; Spratt, Brian G.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 361, Issue 1475
  • DOI: 10.1098/rstb.2006.1917

Competitive strategies differentiate closely related species of marine actinobacteria
journal, August 2015

  • Patin, Nastassia V.; Duncan, Katherine R.; Dorrestein, Pieter C.
  • The ISME Journal, Vol. 10, Issue 2
  • DOI: 10.1038/ismej.2015.128

Competitive strategies differentiate closely related species of marine actinobacteria
journal, August 2015

  • Patin, Nastassia V.; Duncan, Katherine R.; Dorrestein, Pieter C.
  • The ISME Journal, Vol. 10, Issue 2
  • DOI: 10.1038/ismej.2015.128

A comparison of homologous recombination rates in bacteria and archaea
journal, October 2008


A comparison of homologous recombination rates in bacteria and archaea
journal, October 2008


Linking species concepts to natural product discovery in the post-genomic era
journal, December 2009


antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters
journal, May 2015

  • Weber, Tilmann; Blin, Kai; Duddela, Srikanth
  • Nucleic Acids Research, Vol. 43, Issue W1
  • DOI: 10.1093/nar/gkv437

Species-Specific Secondary Metabolite Production in Marine Actinomycetes of the Genus Salinispora
journal, December 2006

  • Jensen, P. R.; Williams, P. G.; Oh, D. -C.
  • Applied and Environmental Microbiology, Vol. 73, Issue 4
  • DOI: 10.1128/aem.01891-06

Linking species concepts to natural product discovery in the post-genomic era
journal, December 2009


Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003


On the origin of prokaryotic species
journal, May 2009


Widespread interspecies homologous recombination reveals reticulate evolution within the genus Streptomyces
journal, September 2016


What are Bacterial Species?
journal, October 2002


Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology.
journal, May 2002

  • Garrity, George M.; Trüper, Hans G.; Whitman, William B.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 52, Issue 3
  • DOI: 10.1099/00207713-52-3-1043

The Bacterial Species Challenge: Making Sense of Genetic and Ecological Diversity
journal, February 2009


ASTRAL: genome-scale coalescent-based species tree estimation
journal, August 2014


Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species.
text, January 2010

  • Donati, Claudio; Hiller, Natalia; Tettelin, Herve
  • Carnegie Mellon University
  • DOI: 10.1184/r1/6104375

Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants
journal, July 2021


Genetic basis for the establishment of endosymbiosis in Paramecium
journal, January 2019


What are Bacterial Species?
journal, October 2002


Recombination and the Nature of Bacterial Speciation
journal, January 2007


Sequences, sequence clusters and bacterial species
journal, October 2006

  • Hanage, William P.; Fraser, Christophe; Spratt, Brian G.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 361, Issue 1475
  • DOI: 10.1098/rstb.2006.1917

Salinispora arenicola gen. nov., sp. nov. and Salinispora tropica sp. nov., obligate marine actinomycetes belonging to the family Micromonosporaceae
journal, September 2005

  • Maldonado, L. A.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 55, Issue 5
  • DOI: 10.1099/ijs.0.63625-0

Multilocus Sequence Typing Reveals Evidence of Homologous Recombination Linked to Antibiotic Resistance in the Genus Salinispora
journal, July 2013

  • Freel, Kelle C.; Millán-Aguiñaga, Natalie; Jensen, Paul R.
  • Applied and Environmental Microbiology, Vol. 79, Issue 19
  • DOI: 10.1128/aem.00880-13

antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters
journal, May 2015

  • Weber, Tilmann; Blin, Kai; Duddela, Srikanth
  • Nucleic Acids Research, Vol. 43, Issue W1
  • DOI: 10.1093/nar/gkv437

The marine actinomycete genus Salinispora: a model organism for secondary metabolite discovery
journal, January 2015

  • Jensen, Paul R.; Moore, Bradley S.; Fenical, William
  • Natural Product Reports, Vol. 32, Issue 5
  • DOI: 10.1039/c4np00167b

Genomic basis for natural product biosynthetic diversity in the actinomycetes
journal, January 2009

  • Nett, Markus; Ikeda, Haruo; Moore, Bradley S.
  • Natural Product Reports, Vol. 26, Issue 11
  • DOI: 10.1039/b817069j

Probing the pan-genome of Listeria monocytogenes: new insights into intraspecific niche expansion and genomic diversification
journal, January 2010


Diversity and evolution of secondary metabolism in the marine actinomycete genus Salinispora
journal, March 2014

  • Ziemert, N.; Lechner, A.; Wietz, M.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 12
  • DOI: 10.1073/pnas.1324161111

Microbial taxonomy in the post-genomic era: Rebuilding from scratch?
journal, December 2014

  • Thompson, Cristiane C.; Amaral, Gilda R.; Campeão, Mariana
  • Archives of Microbiology, Vol. 197, Issue 3
  • DOI: 10.1007/s00203-014-1071-2

Sphingopyxis jiangsuensis sp. nov. Isolated From the Surface Water of the Yellow Sea
journal, June 2022


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

Salinispora pacifica sp. nov., an actinomycete from marine sediments
journal, January 2013


Phylogenomics: Improving Functional Predictions for Uncharacterized Genes by Evolutionary Analysis
journal, March 1998


Diversity and distribution of the bioactive actinobacterial genus Salinispora from sponges along the Great Barrier Reef
journal, November 2011


Widespread interspecies homologous recombination reveals reticulate evolution within the genus Streptomyces
journal, September 2016


Contributions of ancestral inter-species recombination to the genetic diversity of extant Streptomyces lineages
journal, February 2016

  • Andam, Cheryl P.; Choudoir, Mallory J.; Vinh Nguyen, Anh
  • The ISME Journal, Vol. 10, Issue 7
  • DOI: 10.1038/ismej.2015.230

On the origin of prokaryotic species
journal, May 2009


Re-evaluating prokaryotic species
journal, August 2005

  • Gevers, Dirk; Cohan, Frederick M.; Lawrence, Jeffrey G.
  • Nature Reviews Microbiology, Vol. 3, Issue 9
  • DOI: 10.1038/nrmicro1236

RNA polymerase II stalling: loading at the start prepares genes for a sprint
journal, January 2008


Adaptation of Hansenula polymorpha to methanol: a transcriptome analysis
journal, January 2010

  • van Zutphen, Tim; Baerends, Richard JS; Susanna, Kim A.
  • BMC Genomics, Vol. 11, Issue 1
  • DOI: 10.1186/1471-2164-11-1

Genomes of diverse isolates of the marine cyanobacterium Prochlorococcus
journal, September 2014

  • Biller, Steven J.; Berube, Paul M.; Berta-Thompson, Jessie W.
  • Scientific Data, Vol. 1, Issue 1
  • DOI: 10.1038/sdata.2014.34

DNA Sequence Similarity Requirements for Interspecific Recombination in Bacillus
journal, December 1999


Works referencing / citing this record:

Use of genome-scale models to get new insights into the marine actinomycete genus Salinispora
journal, January 2019

  • Contador, Carolina A.; Rodríguez, Vida; Andrews, Barbara A.
  • BMC Systems Biology, Vol. 13, Issue 1
  • DOI: 10.1186/s12918-019-0683-1

Metabolomic Fingerprinting of Salinispora From Atlantic Oceanic Islands
journal, December 2018

  • Bauermeister, Anelize; Velasco-Alzate, Karen; Dias, Tiago
  • Frontiers in Microbiology, Vol. 9
  • DOI: 10.3389/fmicb.2018.03021

Genome-based classification of micromonosporae with a focus on their biotechnological and ecological potential
journal, January 2018


Awakening ancient polar Actinobacteria: diversity, evolution and specialized metabolite potential
journal, November 2019

  • Millán-Aguiñaga, Natalie; Soldatou, Sylvia; Brozio, Sarah
  • Microbiology, Vol. 165, Issue 11
  • DOI: 10.1099/mic.0.000845

Genome-based classification of micromonosporae with a focus on their biotechnological and ecological potential
journal, January 2018