Chromulinavorax destructans, a pathogen of microzooplankton that provides a window into the enigmatic candidate phylum Dependentiae

Members of the major candidate phylum Dependentiae (a.k.a. TM6) are widespread across diverse environments from showerheads to peat bogs; yet, with the exception of two isolates infecting amoebae, they are only known from metagenomic data. The limited knowledge of their biology indicates that they h...

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Vydané v:PLoS pathogens Ročník 15; číslo 5; s. e1007801
Hlavní autori: Deeg, Christoph M., Zimmer, Matthias M., George, Emma E., Husnik, Filip, Keeling, Patrick J., Suttle, Curtis A.
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States Public Library of Science 01.05.2019
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Abstract Members of the major candidate phylum Dependentiae (a.k.a. TM6) are widespread across diverse environments from showerheads to peat bogs; yet, with the exception of two isolates infecting amoebae, they are only known from metagenomic data. The limited knowledge of their biology indicates that they have a long evolutionary history of parasitism. Here, we present Chromulinavorax destructans (Strain SeV1) the first isolate of this phylum to infect a representative from a widespread and ecologically significant group of heterotrophic flagellates, the microzooplankter Spumella elongata (Strain CCAP 955/1). Chromulinavorax destructans has a reduced 1.2 Mb genome that is so specialized for infection that it shows no evidence of complete metabolic pathways, but encodes an extensive transporter system for importing nutrients and energy in the form of ATP from the host. Its replication causes extensive reorganization and expansion of the mitochondrion, effectively surrounding the pathogen, consistent with its dependency on the host for energy. Nearly half (44%) of the inferred proteins contain signal sequences for secretion, including many without recognizable similarity to proteins of known function, as well as 98 copies of proteins with an ankyrin-repeat domain; ankyrin-repeats are known effectors of host modulation, suggesting the presence of an extensive host-manipulation apparatus. These observations help to cement members of this phylum as widespread and diverse parasites infecting a broad range of eukaryotic microbes.
AbstractList Members of the major candidate phylum Dependentiae (a.k.a. TM6) are widespread across diverse environments from showerheads to peat bogs; yet, with the exception of two isolates infecting amoebae, they are only known from metagenomic data. The limited knowledge of their biology indicates that they have a long evolutionary history of parasitism. Here, we present Chromulinavorax destructans (Strain SeV1) the first isolate of this phylum to infect a representative from a widespread and ecologically significant group of heterotrophic flagellates, the microzooplankter Spumella elongata (Strain CCAP 955/1). Chromulinavorax destructans has a reduced 1.2 Mb genome that is so specialized for infection that it shows no evidence of complete metabolic pathways, but encodes an extensive transporter system for importing nutrients and energy in the form of ATP from the host. Its replication causes extensive reorganization and expansion of the mitochondrion, effectively surrounding the pathogen, consistent with its dependency on the host for energy. Nearly half (44%) of the inferred proteins contain signal sequences for secretion, including many without recognizable similarity to proteins of known function, as well as 98 copies of proteins with an ankyrin-repeat domain; ankyrin-repeats are known effectors of host modulation, suggesting the presence of an extensive host-manipulation apparatus. These observations help to cement members of this phylum as widespread and diverse parasites infecting a broad range of eukaryotic microbes.
Members of the major candidate phylum Dependentiae (a.k.a. TM6) are widespread across diverse environments from showerheads to peat bogs; yet, with the exception of two isolates infecting amoebae, they are only known from metagenomic data. The limited knowledge of their biology indicates that they have a long evolutionary history of parasitism. Here, we present Chromulinavorax destructans (Strain SeV1) the first isolate of this phylum to infect a representative from a widespread and ecologically significant group of heterotrophic flagellates, the microzooplankter Spumella elongata (Strain CCAP 955/1). Chromulinavorax destructans has a reduced 1.2 Mb genome that is so specialized for infection that it shows no evidence of complete metabolic pathways, but encodes an extensive transporter system for importing nutrients and energy in the form of ATP from the host. Its replication causes extensive reorganization and expansion of the mitochondrion, effectively surrounding the pathogen, consistent with its dependency on the host for energy. Nearly half (44%) of the inferred proteins contain signal sequences for secretion, including many without recognizable similarity to proteins of known function, as well as 98 copies of proteins with an ankyrin-repeat domain; ankyrin-repeats are known effectors of host modulation, suggesting the presence of an extensive host-manipulation apparatus. These observations help to cement members of this phylum as widespread and diverse parasites infecting a broad range of eukaryotic microbes. Little is known about the biology of bacteria in the candidate phylum Dependentiae, despite being widespread in nature. Here, we describe a novel isolate of this phylum, Chromulinavorax destructans, which infects an abundant aquatic predatory protist, Spumella elongata. Chromulinavorax destructans is an obligate intracellular parasite, forgoes binary fission and replicates surrounded by the host mitochondrion. The genome of C. destructans encodes no detectable complete metabolic pathways and instead contains extensive transporter systems to import metabolites and even energy in the form of ATP from the host. We also found a surprising number of genes in the C. destructans genome encoding putative host modifying proteins that might be responsible for the extensive host reorganization. Phylogenetic analysis showed that C. destructans is distantly related to intracellular pathogens and symbionts of unrelated amoebae. Hence, Chromulinavorax destructans provides new insights into the biology of a widespread but largely unknown phylum of bacteria. These results imply that members of the Dependentiae are pathogens of diverse aquatic protists and are therefore likely important players in aquatic ecosystems.
Members of the major candidate phylum Dependentiae (a.k.a. TM6) are widespread across diverse environments from showerheads to peat bogs; yet, with the exception of two isolates infecting amoebae, they are only known from metagenomic data. The limited knowledge of their biology indicates that they have a long evolutionary history of parasitism. Here, we present Chromulinavorax destructans (Strain SeV1) the first isolate of this phylum to infect a representative from a widespread and ecologically significant group of heterotrophic flagellates, the microzooplankter Spumella elongata (Strain CCAP 955/1). Chromulinavorax destructans has a reduced 1.2 Mb genome that is so specialized for infection that it shows no evidence of complete metabolic pathways, but encodes an extensive transporter system for importing nutrients and energy in the form of ATP from the host. Its replication causes extensive reorganization and expansion of the mitochondrion, effectively surrounding the pathogen, consistent with its dependency on the host for energy. Nearly half (44%) of the inferred proteins contain signal sequences for secretion, including many without recognizable similarity to proteins of known function, as well as 98 copies of proteins with an ankyrin-repeat domain; ankyrin-repeats are known effectors of host modulation, suggesting the presence of an extensive host-manipulation apparatus. These observations help to cement members of this phylum as widespread and diverse parasites infecting a broad range of eukaryotic microbes.Members of the major candidate phylum Dependentiae (a.k.a. TM6) are widespread across diverse environments from showerheads to peat bogs; yet, with the exception of two isolates infecting amoebae, they are only known from metagenomic data. The limited knowledge of their biology indicates that they have a long evolutionary history of parasitism. Here, we present Chromulinavorax destructans (Strain SeV1) the first isolate of this phylum to infect a representative from a widespread and ecologically significant group of heterotrophic flagellates, the microzooplankter Spumella elongata (Strain CCAP 955/1). Chromulinavorax destructans has a reduced 1.2 Mb genome that is so specialized for infection that it shows no evidence of complete metabolic pathways, but encodes an extensive transporter system for importing nutrients and energy in the form of ATP from the host. Its replication causes extensive reorganization and expansion of the mitochondrion, effectively surrounding the pathogen, consistent with its dependency on the host for energy. Nearly half (44%) of the inferred proteins contain signal sequences for secretion, including many without recognizable similarity to proteins of known function, as well as 98 copies of proteins with an ankyrin-repeat domain; ankyrin-repeats are known effectors of host modulation, suggesting the presence of an extensive host-manipulation apparatus. These observations help to cement members of this phylum as widespread and diverse parasites infecting a broad range of eukaryotic microbes.
Audience Academic
Author Zimmer, Matthias M.
Suttle, Curtis A.
Deeg, Christoph M.
George, Emma E.
Keeling, Patrick J.
Husnik, Filip
AuthorAffiliation 2 Department of Earth, Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, Canada
3 Department of Botany, University of British Columbia, Vancouver, Canada
1 Department of Microbiology and Immunology, University of British Columbia, Vancouver, Canada
Pennsylvania State University, UNITED STATES
4 Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, Canada
AuthorAffiliation_xml – name: 2 Department of Earth, Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, Canada
– name: 1 Department of Microbiology and Immunology, University of British Columbia, Vancouver, Canada
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– name: Pennsylvania State University, UNITED STATES
– name: 4 Institute for the Oceans and Fisheries, University of British Columbia, Vancouver, Canada
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  givenname: Christoph M.
  orcidid: 0000-0002-4459-9372
  surname: Deeg
  fullname: Deeg, Christoph M.
– sequence: 2
  givenname: Matthias M.
  surname: Zimmer
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  givenname: Emma E.
  surname: George
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/31150530$$D View this record in MEDLINE/PubMed
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Snippet Members of the major candidate phylum Dependentiae (a.k.a. TM6) are widespread across diverse environments from showerheads to peat bogs; yet, with the...
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StartPage e1007801
SubjectTerms Amoeba
Animals
Ankyrins
Atmospheric sciences
Bacteria
Bacteria - classification
Bacteria - genetics
Bacteria - pathogenicity
Bioinformatics
Biological evolution
Biology
Biology and Life Sciences
Bogs
Chrysophyta - microbiology
Computer and Information Sciences
Dependence
Flagellates
Flow cytometry
Genes
Genetic aspects
Genome, Bacterial
Genomes
Host Microbial Interactions
Host-bacteria relationships
Immunology
Infections
Integrated software
Metabolic pathways
Microscopy
Nutrients
Parasites
Parasitism
Pathogens
Peat
Peat bogs
Phylogenetics
Phylogeny
Physiological aspects
Proteins
Research and Analysis Methods
Secretion
Supervision
Viruses
Zooplankton
Zooplankton - microbiology
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Title Chromulinavorax destructans, a pathogen of microzooplankton that provides a window into the enigmatic candidate phylum Dependentiae
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Volume 15
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