Complete Genome of a Member of a New Bacterial Lineage in the Microgenomates Group Reveals an Unusual Nucleotide Composition Disparity Between Two Strands of DNA and Limited Metabolic Potential

The candidate phyla radiation is a large monophyletic lineage comprising unculturable bacterial taxa with small cell and genome sizes, mostly known from genomes obtained from environmental sources without cultivation. Here, we present the closed complete genome of a member of the superphylum Microge...

Full description

Bibliographic Details
Main Authors: Vitaly V. Kadnikov, Andrey V. Mardanov, Alexey V. Beletsky, Olga V. Karnachuk, Nikolai V. Ravin
Format: Article
Language:English
Published: MDPI AG 2020-02-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/8/3/320
_version_ 1818851331591372800
author Vitaly V. Kadnikov
Andrey V. Mardanov
Alexey V. Beletsky
Olga V. Karnachuk
Nikolai V. Ravin
author_facet Vitaly V. Kadnikov
Andrey V. Mardanov
Alexey V. Beletsky
Olga V. Karnachuk
Nikolai V. Ravin
author_sort Vitaly V. Kadnikov
collection DOAJ
description The candidate phyla radiation is a large monophyletic lineage comprising unculturable bacterial taxa with small cell and genome sizes, mostly known from genomes obtained from environmental sources without cultivation. Here, we present the closed complete genome of a member of the superphylum Microgenomates obtained from the metagenome of a deep subsurface thermal aquifer. Phylogenetic analysis indicates that the new bacterium, designated Ch65, represents a novel phylum-level lineage within the Microgenomates group, sibling to the candidate phylum Collierbacteria. The Ch65 genome has a highly unusual nucleotide composition with one strand of highly enriched in cytosine versus guanine throughout the whole length. Such nucleotide composition asymmetry, also detected in the members of Ca. Collierbacteria and Ca. Beckwithbacteria, suggests that most of the Ch65 chromosome is replicated in one direction. A genome analysis predicted that the Ch65 bacterium has fermentative metabolism and could produce acetate and lactate. It lacks respiratory capacity, as well as complete pathways for the biosynthesis of lipids, amino acids, and nucleotides. The Embden&#8722;Meyerhof glycolytic pathway and nonoxidative pentose phosphate pathway are mostly complete, although glucokinase, 6-phosphofructokinase, and transaldolase were not found. The Ch65 bacterium lacks secreted glycoside hydrolases and conventional transporters for importing sugars and amino acids. Overall, the metabolic predictions imply that Ch65 adopts the lifestyle of a symbiont/parasite, or a scavenger, obtaining resources from the lysed microbial biomass. We propose the provisional taxonomic assignment &#8216;<i>Candidatus</i> Chazhemtobacterium aquaticus&#8217;, genus &#8216;<i>Chazhemtobacterium</i>&#8216;, family &#8216;<i>Chazhemtobacteraceae</i>&#8216; in the Microgenomates group.
first_indexed 2024-12-19T07:03:20Z
format Article
id doaj.art-113ed30e899f4bc6b1b11a21744ae35c
institution Directory Open Access Journal
issn 2076-2607
language English
last_indexed 2024-12-19T07:03:20Z
publishDate 2020-02-01
publisher MDPI AG
record_format Article
series Microorganisms
spelling doaj.art-113ed30e899f4bc6b1b11a21744ae35c2022-12-21T20:31:22ZengMDPI AGMicroorganisms2076-26072020-02-018332010.3390/microorganisms8030320microorganisms8030320Complete Genome of a Member of a New Bacterial Lineage in the Microgenomates Group Reveals an Unusual Nucleotide Composition Disparity Between Two Strands of DNA and Limited Metabolic PotentialVitaly V. Kadnikov0Andrey V. Mardanov1Alexey V. Beletsky2Olga V. Karnachuk3Nikolai V. Ravin4Institute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow 119071, RussiaInstitute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow 119071, RussiaInstitute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow 119071, RussiaLaboratory of Biochemistry and Molecular Biology, Tomsk State University, Tomsk 634050, RussiaInstitute of Bioengineering, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow 119071, RussiaThe candidate phyla radiation is a large monophyletic lineage comprising unculturable bacterial taxa with small cell and genome sizes, mostly known from genomes obtained from environmental sources without cultivation. Here, we present the closed complete genome of a member of the superphylum Microgenomates obtained from the metagenome of a deep subsurface thermal aquifer. Phylogenetic analysis indicates that the new bacterium, designated Ch65, represents a novel phylum-level lineage within the Microgenomates group, sibling to the candidate phylum Collierbacteria. The Ch65 genome has a highly unusual nucleotide composition with one strand of highly enriched in cytosine versus guanine throughout the whole length. Such nucleotide composition asymmetry, also detected in the members of Ca. Collierbacteria and Ca. Beckwithbacteria, suggests that most of the Ch65 chromosome is replicated in one direction. A genome analysis predicted that the Ch65 bacterium has fermentative metabolism and could produce acetate and lactate. It lacks respiratory capacity, as well as complete pathways for the biosynthesis of lipids, amino acids, and nucleotides. The Embden&#8722;Meyerhof glycolytic pathway and nonoxidative pentose phosphate pathway are mostly complete, although glucokinase, 6-phosphofructokinase, and transaldolase were not found. The Ch65 bacterium lacks secreted glycoside hydrolases and conventional transporters for importing sugars and amino acids. Overall, the metabolic predictions imply that Ch65 adopts the lifestyle of a symbiont/parasite, or a scavenger, obtaining resources from the lysed microbial biomass. We propose the provisional taxonomic assignment &#8216;<i>Candidatus</i> Chazhemtobacterium aquaticus&#8217;, genus &#8216;<i>Chazhemtobacterium</i>&#8216;, family &#8216;<i>Chazhemtobacteraceae</i>&#8216; in the Microgenomates group.https://www.mdpi.com/2076-2607/8/3/320candidate phyla radiationmicrogenomatesmetagenomicscomplete genomedna replication
spellingShingle Vitaly V. Kadnikov
Andrey V. Mardanov
Alexey V. Beletsky
Olga V. Karnachuk
Nikolai V. Ravin
Complete Genome of a Member of a New Bacterial Lineage in the Microgenomates Group Reveals an Unusual Nucleotide Composition Disparity Between Two Strands of DNA and Limited Metabolic Potential
Microorganisms
candidate phyla radiation
microgenomates
metagenomics
complete genome
dna replication
title Complete Genome of a Member of a New Bacterial Lineage in the Microgenomates Group Reveals an Unusual Nucleotide Composition Disparity Between Two Strands of DNA and Limited Metabolic Potential
title_full Complete Genome of a Member of a New Bacterial Lineage in the Microgenomates Group Reveals an Unusual Nucleotide Composition Disparity Between Two Strands of DNA and Limited Metabolic Potential
title_fullStr Complete Genome of a Member of a New Bacterial Lineage in the Microgenomates Group Reveals an Unusual Nucleotide Composition Disparity Between Two Strands of DNA and Limited Metabolic Potential
title_full_unstemmed Complete Genome of a Member of a New Bacterial Lineage in the Microgenomates Group Reveals an Unusual Nucleotide Composition Disparity Between Two Strands of DNA and Limited Metabolic Potential
title_short Complete Genome of a Member of a New Bacterial Lineage in the Microgenomates Group Reveals an Unusual Nucleotide Composition Disparity Between Two Strands of DNA and Limited Metabolic Potential
title_sort complete genome of a member of a new bacterial lineage in the microgenomates group reveals an unusual nucleotide composition disparity between two strands of dna and limited metabolic potential
topic candidate phyla radiation
microgenomates
metagenomics
complete genome
dna replication
url https://www.mdpi.com/2076-2607/8/3/320
work_keys_str_mv AT vitalyvkadnikov completegenomeofamemberofanewbacteriallineageinthemicrogenomatesgrouprevealsanunusualnucleotidecompositiondisparitybetweentwostrandsofdnaandlimitedmetabolicpotential
AT andreyvmardanov completegenomeofamemberofanewbacteriallineageinthemicrogenomatesgrouprevealsanunusualnucleotidecompositiondisparitybetweentwostrandsofdnaandlimitedmetabolicpotential
AT alexeyvbeletsky completegenomeofamemberofanewbacteriallineageinthemicrogenomatesgrouprevealsanunusualnucleotidecompositiondisparitybetweentwostrandsofdnaandlimitedmetabolicpotential
AT olgavkarnachuk completegenomeofamemberofanewbacteriallineageinthemicrogenomatesgrouprevealsanunusualnucleotidecompositiondisparitybetweentwostrandsofdnaandlimitedmetabolicpotential
AT nikolaivravin completegenomeofamemberofanewbacteriallineageinthemicrogenomatesgrouprevealsanunusualnucleotidecompositiondisparitybetweentwostrandsofdnaandlimitedmetabolicpotential