Cultivation and Complete Genome Sequencing of Gloeobacter kilaueensis sp. nov., from a Lava Cave in Kīlauea Caldera, Hawai'i

The ancestor of Gloeobacter violaceus PCC 7421T is believed to have diverged from that of all known cyanobacteria before the evolution of thylakoid membranes and plant plastids. The long and largely independent evolutionary history of G. violaceus presents an organism retaining ancestral features of early oxygenic photoautotrophs, and in whom cyanobacteria evolution can be investigated. No other Gloeobacter species has been described since the genus was established in 1974 (Rippka et al., Arch Microbiol 100:435). Gloeobacter affiliated ribosomal gene sequences have been reported in environmental DNA libraries, but only the type strain's genome has been sequenced. However, we report here the cultivation of a new Gloeobacter species, G. kilaueensis JS1T, from an epilithic biofilm in a lava cave in Kīlauea Caldera, Hawai'i. The strain's genome was sequenced from an enriched culture resembling a low-complexity metagenomic sample, using 9 kb paired-end 454 pyrosequences and 400 bp paired-end Illumina reads. The JS1T and G. violaceus PCC 7421T genomes have little gene synteny despite sharing 2842 orthologous genes; comparing the genomes shows they do not belong to the same species. Our results support establishing a new species to accommodate JS1T, for which we propose the name Gloeobacter kilaueensis sp. nov. Strain JS1T has been deposited in the American Type Culture Collection (BAA-2537), the Scottish Marine Institute's Culture Collection of Algae and Protozoa (CCAP 1431/1), and the Belgian Coordinated Collections of Microorganisms (ULC0316). The G. kilaueensis holotype has been deposited in the Algal Collection of the US National Herbarium (US# 217948). The JS1T genome sequence has been deposited in GenBank under accession number CP003587. The G+C content of the genome is 60.54 mol%. The complete genome sequence of G. kilaueensis JS1T may further understanding of cyanobacteria evolution, and the shift from anoxygenic to oxygenic photosynthesis.

[1]  O. Strunecký,et al.  The Primitive Thylakoid-Less Cyanobacterium Gloeobacter Is a Common Rock-Dwelling Organism , 2013, PloS one.

[2]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[3]  Bettina E. Schirrmeister,et al.  Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event , 2013, Proceedings of the National Academy of Sciences.

[4]  D. Moreira,et al.  An Early-Branching Microbialite Cyanobacterium Forms Intracellular Carbonates , 2012, Science.

[5]  M. Alam,et al.  Complete genome sequencing and analysis of Saprospira grandis str. Lewin, a predatory marine bacterium , 2012, Standards in genomic sciences.

[6]  M. Suchard,et al.  Bayesian Phylogenetics with BEAUti and the BEAST 1.7 , 2012, Molecular biology and evolution.

[7]  J. McNeill,et al.  Major changes to theCode of Nomenclature-Melbourne, July 2011 , 2011 .

[8]  H. Klenk,et al.  Relationship of Bacillus amyloliquefaciens clades associated with strains DSM 7T and FZB42T: a proposal for Bacillus amyloliquefaciens subsp. amyloliquefaciens subsp. nov. and Bacillus amyloliquefaciens subsp. plantarum subsp. nov. based on complete genome sequence comparisons. , 2011, International journal of systematic and evolutionary microbiology.

[9]  H. Frank,et al.  Configuration of spheroidene in the photosynthetic reaction center of Rhodobacter sphaeroides : a comparison of wild-type and reconstituted R26. , 2011, The journal of physical chemistry. A.

[10]  Stan J. J. Brouns,et al.  Evolution and classification of the CRISPR–Cas systems , 2011, Nature Reviews Microbiology.

[11]  C. Mullineaux,et al.  The Plasma Membrane of the Cyanobacterium Gloeobacter violaceus Contains Segregated Bioenergetic Domains[C][W] , 2011, Plant Cell.

[12]  S. Salzberg,et al.  PhymmBL expanded: confidence scores, custom databases, parallelization and more , 2011, Nature Methods.

[13]  Alexandre Antonelli,et al.  The origin of multicellularity in cyanobacteria , 2011, BMC Evolutionary Biology.

[14]  Tal Pupko,et al.  GLOOME: gain loss mapping engine , 2010, Bioinform..

[15]  H. Deveau,et al.  CRISPR/Cas system and its role in phage-bacteria interactions. , 2010, Annual review of microbiology.

[16]  L. D'Acqui,et al.  Biodiversity of Phototrophic Biofilms Dwelling on Monumental Fountains , 2010, Microbial Ecology.

[17]  Hans-Peter Klenk,et al.  Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison , 2010, Standards in genomic sciences.

[18]  Tal Pupko,et al.  Inference and Characterization of Horizontally Transferred Gene Families Using Stochastic Mapping , 2009, Molecular biology and evolution.

[19]  J. Williams,et al.  The evolutionary pathway from anoxygenic to oxygenic photosynthesis examined by comparison of the properties of photosystem II and bacterial reaction centers , 2010, Photosynthesis Research.

[20]  Miriam L. Land,et al.  Trace: Tennessee Research and Creative Exchange Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification Recommended Citation Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification , 2022 .

[21]  R. Rosselló-Móra,et al.  Shifting the genomic gold standard for the prokaryotic species definition , 2009, Proceedings of the National Academy of Sciences.

[22]  J. Peter Gogarten,et al.  Intertwined Evolutionary Histories of Marine Synechococcus and Prochlorococcus marinus , 2009, Genome biology and evolution.

[23]  Steven J. M. Jones,et al.  Circos: an information aesthetic for comparative genomics. , 2009, Genome research.

[24]  S. Salzberg,et al.  Phymm and PhymmBL: Metagenomic Phylogenetic Classification with Interpolated Markov Models , 2009, Nature Methods.

[25]  Toni Gabaldón,et al.  trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses , 2009, Bioinform..

[26]  W. Nelson,et al.  Germ Warfare in a Microbial Mat Community: CRISPRs Provide Insights into the Co-Evolution of Host and Viral Genomes , 2009, PloS one.

[27]  M. Mimuro,et al.  Two unique cyanobacteria lead to a traceable approach of the first appearance of oxygenic photosynthesis , 2008, Photosynthesis Research.

[28]  P. Wincker,et al.  Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria , 2008, Genome Biology.

[29]  E. Birney,et al.  Velvet: algorithms for de novo short read assembly using de Bruijn graphs. , 2008, Genome research.

[30]  E. Flores,et al.  The cyanobacteria : molecular biology, genomics, and evolution , 2008 .

[31]  P. Vandamme,et al.  DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. , 2007, International journal of systematic and evolutionary microbiology.

[32]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[33]  Maureen L. Coleman,et al.  Genomic Islands and the Ecology and Evolution of Prochlorococcus , 2006, Science.

[34]  Ramon Rosselló-Móra,et al.  DNA-DNA Reassociation Methods Applied to Microbial Taxonomy and Their Critical Evaluation , 2006 .

[35]  Patrice Courvalin,et al.  Vancomycin resistance in gram-positive cocci. , 2006, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[36]  G. Sandmann,et al.  Carotenoid biosynthesis in Gloeobacter violaceus PCC4721 involves a single crtI-type phytoene desaturase instead of typical cyanobacterial enzymes , 2005, Archives of Microbiology.

[37]  M. Mimuro,et al.  The cyanobacterium Gloeobacter violaceus PCC 7421 uses bacterial‐type phytoene desaturase in carotenoid biosynthesis , 2005, FEBS letters.

[38]  K. Konstantinidis,et al.  Genomic insights that advance the species definition for prokaryotes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[39]  R. Bidigare,et al.  Analysis of Algal Pigments by High-Performance Liquid Chromatography , 2005 .

[40]  Robert C. Edgar,et al.  MUSCLE: a multiple sequence alignment method with reduced time and space complexity , 2004, BMC Bioinformatics.

[41]  J. Waterbury,et al.  A cyanobacterium which lacks thylakoids , 2004, Archives of Microbiology.

[42]  S. Salzberg,et al.  Versatile and open software for comparing large genomes , 2004, Genome Biology.

[43]  C. Stoeckert,et al.  OrthoMCL: identification of ortholog groups for eukaryotic genomes. , 2003, Genome research.

[44]  M. Mimuro,et al.  Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. , 2003, DNA research : an international journal for rapid publication of reports on genes and genomes.

[45]  Peter Westhoff,et al.  VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[46]  U. Vothknecht,et al.  Vipp1 deletion mutant of Synechocystis: A connection between bacterial phage shock and thylakoid biogenesis? , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[47]  B. Weisblum,et al.  Peptide analogues of the VanS catalytic center inhibit VanR binding to its cognate promoter. , 2000, Biochemistry.

[48]  C. Benning,et al.  A Cyanobacterial Gene, sqdX, Required for Biosynthesis of the Sulfolipid Sulfoquinovosyldiacylglycerol , 2000, Journal of bacteriology.

[49]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.

[50]  J. Palmer,et al.  Investigating Deep Phylogenetic Relationships among Cyanobacteria and Plastids by Small Subunit rRNA Sequence Analysis 1 , 1999, The Journal of eukaryotic microbiology.

[51]  Gapped BLAST and PSI-BLAST: A new , 1997 .

[52]  C. Benning,et al.  A Null Mutant of Synechococcus sp. PCC7942 Deficient in the Sulfolipid Sulfoquinovosyl Diacylglycerol (*) , 1996, The Journal of Biological Chemistry.

[53]  R. Wachter,et al.  An early origin of plastids within the cyanobacterial divergence is suggested by evolutionary trees based on complete 16S rRNA sequences. , 1995, Molecular biology and evolution.

[54]  C. Walsh,et al.  Identification of the DNA-binding site for the phosphorylated VanR protein required for vancomycin resistance in Enterococcus faecium. , 1994, Biochemistry.

[55]  Sp Lapage,et al.  International Code of Nomenclature of Bacteria: Bacteriological Code, 1990 Revision , 1992 .

[56]  D. Lane 16S/23S rRNA sequencing , 1991 .

[57]  E. Stackebrandt,et al.  Nucleic acid techniques in bacterial systematics , 1991 .

[58]  N. Ryan International Code of Nomenclature of Bacteria. Bacteriological Code , 1977 .