Analysis of five complete genome sequences for members of the class Peribacteria in the recently recognized Peregrinibacteria bacterial phylum

Five closely related populations of bacteria from the Candidate Phylum (CP) Peregrinibacteria, part of the bacterial Candidate Phyla Radiation (CPR), were sampled from filtered groundwater obtained from an aquifer adjacent to the Colorado River near the town of Rifle, CO, USA. Here, we present the first complete genome sequences for organisms from this phylum. These bacteria have small genomes and, unlike most organisms from other lineages in the CPR, have the capacity for nucleotide synthesis. They invest significantly in biosynthesis of cell wall and cell envelope components, including peptidoglycan, isoprenoids via the mevalonate pathway, and a variety of amino sugars including perosamine and rhamnose. The genomes encode an intriguing set of large extracellular proteins, some of which are very cysteine-rich and may function in attachment, possibly to other cells. Strain variation in these proteins is an important source of genotypic variety. Overall, the cell envelope features, combined with the lack of biosynthesis capacities for many required cofactors, fatty acids, and most amino acids point to a symbiotic lifestyle. Phylogenetic analyses indicate that these bacteria likely represent a new class within the Peregrinibacteria phylum, although they ultimately may be recognized as members of a separate phylum. We propose the provisional taxonomic assignment as ‘Candidatus Peribacter riflensis’, Genus Peribacter, Family Peribacteraceae, Order Peribacterales, Class Peribacteria in the phylum Peregrinibacteria.

[1]  Brian C. Thomas,et al.  Metagenomic analysis of a high carbon dioxide subsurface microbial community populated by chemolithoautotrophs and bacteria and archaea from candidate phyla. , 2016, Environmental microbiology.

[2]  Brian C. Thomas,et al.  Unusual biology across a group comprising more than 15% of domain Bacteria , 2015, Nature.

[3]  Brian C. Thomas,et al.  Diverse uncultivated ultra-small bacterial cells in groundwater , 2015, Nature Communications.

[4]  L. Hug,et al.  Aquifer environment selects for microbial species cohorts in sediment and groundwater , 2015, The ISME Journal.

[5]  Robert D. Finn,et al.  Rfam 12.0: updates to the RNA families database , 2014, Nucleic Acids Res..

[6]  Matthew Fraser,et al.  InterProScan 5: genome-scale protein function classification , 2014, Bioinform..

[7]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[8]  M. Savageau,et al.  Relative Amino Acid Composition Signatures of Organisms and Environments , 2013, PloS one.

[9]  Brian C. Thomas,et al.  Small Genomes and Sparse Metabolisms of Sediment-Associated Bacteria from Four Candidate Phyla , 2013, mBio.

[10]  H. Nakayama,et al.  Lipoproteins in bacteria: structures and biosynthetic pathways , 2012, The FEBS journal.

[11]  Brian C. Thomas,et al.  Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla , 2012, Science.

[12]  Siu-Ming Yiu,et al.  IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth , 2012, Bioinform..

[13]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[14]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[15]  James A. Davis,et al.  Acetate Availability and its Influence on Sustainable Bioremediation of Uranium-Contaminated Groundwater , 2011 .

[16]  Daniel R Zerbino,et al.  Using the Velvet de novo Assembler for Short‐Read Sequencing Technologies , 2010, Current protocols in bioinformatics.

[17]  Martin Ester,et al.  PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes , 2010, Bioinform..

[18]  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 .

[19]  Brian C. Thomas,et al.  Community-wide analysis of microbial genome sequence signatures , 2009, Genome Biology.

[20]  Stijn van Dongen,et al.  Graph Clustering Via a Discrete Uncoupling Process , 2008, SIAM J. Matrix Anal. Appl..

[21]  W. Ludwig,et al.  SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB , 2007, Nucleic acids research.

[22]  P. Bork,et al.  Prediction of effective genome size in metagenomic samples , 2007, Genome Biology.

[23]  J. Breznak,et al.  Folate Cross-Feeding Supports Symbiotic Homoacetogenic Spirochetes , 2005, Applied and Environmental Microbiology.

[24]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[25]  S. Mazmanian,et al.  Sortase‐catalysed anchoring of surface proteins to the cell wall of Staphylococcus aureus , 2001, Molecular microbiology.

[26]  David Moreira,et al.  Origins and early evolution of the mevalonate pathway of isoprenoid biosynthesis in the three domains of life. , 2011, Molecular biology and evolution.

[27]  Robert C. Edgar,et al.  Search and clustering orders of magnitude faster than BLAST , 2010 .

[28]  Peter B. McGarvey,et al.  UniRef: comprehensive and non-redundant UniProt reference clusters , 2007, Bioinform..

[29]  Hiroyuki Ogata,et al.  KEGG: Kyoto Encyclopedia of Genes and Genomes , 1999, Nucleic Acids Res..

[30]  BIOINFORMATICS ORIGINAL PAPER doi:10.1093/bioinformatics/btm098 Databases and ontologies UniRef: comprehensive and non-redundant UniProt reference , 2022 .