Cargando…

The Subcellular Proteome of a Planctomycetes Bacterium Shows That Newly Evolved Proteins Have Distinct Fractionation Patterns

The Planctomycetes bacteria have unique cell architectures with heavily invaginated membranes as confirmed by three-dimensional models reconstructed from FIB-SEM images of Tuwongella immobilis and Gemmata obscuriglobus. The subcellular proteome of T. immobilis was examined by differential solubiliza...

Descripción completa

Detalles Bibliográficos
Autores principales: Seeger, Christian, Dyrhage, Karl, Mahajan, Mayank, Odelgard, Anna, Lind, Sara Bergström, Andersson, Siv G. E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8567305/
https://www.ncbi.nlm.nih.gov/pubmed/34745019
http://dx.doi.org/10.3389/fmicb.2021.643045
_version_ 1784594203290894336
author Seeger, Christian
Dyrhage, Karl
Mahajan, Mayank
Odelgard, Anna
Lind, Sara Bergström
Andersson, Siv G. E.
author_facet Seeger, Christian
Dyrhage, Karl
Mahajan, Mayank
Odelgard, Anna
Lind, Sara Bergström
Andersson, Siv G. E.
author_sort Seeger, Christian
collection PubMed
description The Planctomycetes bacteria have unique cell architectures with heavily invaginated membranes as confirmed by three-dimensional models reconstructed from FIB-SEM images of Tuwongella immobilis and Gemmata obscuriglobus. The subcellular proteome of T. immobilis was examined by differential solubilization followed by LC-MS/MS analysis, which identified 1569 proteins in total. The Tris-soluble fraction contained mostly cytoplasmic proteins, while inner and outer membrane proteins were found in the Triton X-100 and SDS-soluble fractions, respectively. For comparisons, the subcellular proteome of Escherichia coli was also examined using the same methodology. A notable difference in the overall fractionation pattern of the two species was a fivefold higher number of predicted cytoplasmic proteins in the SDS-soluble fraction in T. immobilis. One category of such proteins is represented by innovations in the Planctomycetes lineage, including unique sets of serine/threonine kinases and extracytoplasmic sigma factors with WD40 repeat domains for which no homologs are present in E. coli. Other such proteins are members of recently expanded protein families in which the newly evolved paralog with a new domain structure is recovered from the SDS-soluble fraction, while other paralogs may have similar domain structures and fractionation patterns as the single homolog in E. coli. The expanded protein families in T. immobilis include enzymes involved in replication-repair processes as well as in rRNA and tRNA modification and degradation. These results show that paralogization and domain shuffling have yielded new proteins with distinct fractionation characteristics. Understanding the molecular intricacies of these adaptive changes might aid in the development of a model for the evolution of cellular complexity.
format Online
Article
Text
id pubmed-8567305
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-85673052021-11-05 The Subcellular Proteome of a Planctomycetes Bacterium Shows That Newly Evolved Proteins Have Distinct Fractionation Patterns Seeger, Christian Dyrhage, Karl Mahajan, Mayank Odelgard, Anna Lind, Sara Bergström Andersson, Siv G. E. Front Microbiol Microbiology The Planctomycetes bacteria have unique cell architectures with heavily invaginated membranes as confirmed by three-dimensional models reconstructed from FIB-SEM images of Tuwongella immobilis and Gemmata obscuriglobus. The subcellular proteome of T. immobilis was examined by differential solubilization followed by LC-MS/MS analysis, which identified 1569 proteins in total. The Tris-soluble fraction contained mostly cytoplasmic proteins, while inner and outer membrane proteins were found in the Triton X-100 and SDS-soluble fractions, respectively. For comparisons, the subcellular proteome of Escherichia coli was also examined using the same methodology. A notable difference in the overall fractionation pattern of the two species was a fivefold higher number of predicted cytoplasmic proteins in the SDS-soluble fraction in T. immobilis. One category of such proteins is represented by innovations in the Planctomycetes lineage, including unique sets of serine/threonine kinases and extracytoplasmic sigma factors with WD40 repeat domains for which no homologs are present in E. coli. Other such proteins are members of recently expanded protein families in which the newly evolved paralog with a new domain structure is recovered from the SDS-soluble fraction, while other paralogs may have similar domain structures and fractionation patterns as the single homolog in E. coli. The expanded protein families in T. immobilis include enzymes involved in replication-repair processes as well as in rRNA and tRNA modification and degradation. These results show that paralogization and domain shuffling have yielded new proteins with distinct fractionation characteristics. Understanding the molecular intricacies of these adaptive changes might aid in the development of a model for the evolution of cellular complexity. Frontiers Media S.A. 2021-05-04 /pmc/articles/PMC8567305/ /pubmed/34745019 http://dx.doi.org/10.3389/fmicb.2021.643045 Text en Copyright © 2021 Seeger, Dyrhage, Mahajan, Odelgard, Lind and Andersson. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Seeger, Christian
Dyrhage, Karl
Mahajan, Mayank
Odelgard, Anna
Lind, Sara Bergström
Andersson, Siv G. E.
The Subcellular Proteome of a Planctomycetes Bacterium Shows That Newly Evolved Proteins Have Distinct Fractionation Patterns
title The Subcellular Proteome of a Planctomycetes Bacterium Shows That Newly Evolved Proteins Have Distinct Fractionation Patterns
title_full The Subcellular Proteome of a Planctomycetes Bacterium Shows That Newly Evolved Proteins Have Distinct Fractionation Patterns
title_fullStr The Subcellular Proteome of a Planctomycetes Bacterium Shows That Newly Evolved Proteins Have Distinct Fractionation Patterns
title_full_unstemmed The Subcellular Proteome of a Planctomycetes Bacterium Shows That Newly Evolved Proteins Have Distinct Fractionation Patterns
title_short The Subcellular Proteome of a Planctomycetes Bacterium Shows That Newly Evolved Proteins Have Distinct Fractionation Patterns
title_sort subcellular proteome of a planctomycetes bacterium shows that newly evolved proteins have distinct fractionation patterns
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8567305/
https://www.ncbi.nlm.nih.gov/pubmed/34745019
http://dx.doi.org/10.3389/fmicb.2021.643045
work_keys_str_mv AT seegerchristian thesubcellularproteomeofaplanctomycetesbacteriumshowsthatnewlyevolvedproteinshavedistinctfractionationpatterns
AT dyrhagekarl thesubcellularproteomeofaplanctomycetesbacteriumshowsthatnewlyevolvedproteinshavedistinctfractionationpatterns
AT mahajanmayank thesubcellularproteomeofaplanctomycetesbacteriumshowsthatnewlyevolvedproteinshavedistinctfractionationpatterns
AT odelgardanna thesubcellularproteomeofaplanctomycetesbacteriumshowsthatnewlyevolvedproteinshavedistinctfractionationpatterns
AT lindsarabergstrom thesubcellularproteomeofaplanctomycetesbacteriumshowsthatnewlyevolvedproteinshavedistinctfractionationpatterns
AT anderssonsivge thesubcellularproteomeofaplanctomycetesbacteriumshowsthatnewlyevolvedproteinshavedistinctfractionationpatterns
AT seegerchristian subcellularproteomeofaplanctomycetesbacteriumshowsthatnewlyevolvedproteinshavedistinctfractionationpatterns
AT dyrhagekarl subcellularproteomeofaplanctomycetesbacteriumshowsthatnewlyevolvedproteinshavedistinctfractionationpatterns
AT mahajanmayank subcellularproteomeofaplanctomycetesbacteriumshowsthatnewlyevolvedproteinshavedistinctfractionationpatterns
AT odelgardanna subcellularproteomeofaplanctomycetesbacteriumshowsthatnewlyevolvedproteinshavedistinctfractionationpatterns
AT lindsarabergstrom subcellularproteomeofaplanctomycetesbacteriumshowsthatnewlyevolvedproteinshavedistinctfractionationpatterns
AT anderssonsivge subcellularproteomeofaplanctomycetesbacteriumshowsthatnewlyevolvedproteinshavedistinctfractionationpatterns