Interspecies Microbial Fusion and Large-Scale Exchange of Cytoplasmic Proteins and RNA in a Syntrophic <italic toggle="yes">Clostridium</italic> Coculture

ABSTRACT Microbial syntrophy is universal in nature, profoundly affecting the composition and function of microbiomes. We have recently reported data suggesting direct cell-to-cell interactions leading to electron and material exchange between the two microbes in the syntrophy between Clostridium lj...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Kamil Charubin, Shannon Modla, Jeffrey L. Caplan, Eleftherios Terry Papoutsakis
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://doaj.org/article/ffc00ad7c5994fcb97d7b07713c744e4
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:ffc00ad7c5994fcb97d7b07713c744e4
record_format dspace
spelling oai:doaj.org-article:ffc00ad7c5994fcb97d7b07713c744e42021-11-15T16:19:09ZInterspecies Microbial Fusion and Large-Scale Exchange of Cytoplasmic Proteins and RNA in a Syntrophic <italic toggle="yes">Clostridium</italic> Coculture10.1128/mBio.02030-202150-7511https://doaj.org/article/ffc00ad7c5994fcb97d7b07713c744e42020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02030-20https://doaj.org/toc/2150-7511ABSTRACT Microbial syntrophy is universal in nature, profoundly affecting the composition and function of microbiomes. We have recently reported data suggesting direct cell-to-cell interactions leading to electron and material exchange between the two microbes in the syntrophy between Clostridium ljungdahlii and C. acetobutylicum. Here, transmission electron microscopy and electron tomography demonstrated cell wall and membrane fusions between the two organisms, whereby C. ljungdahlii appears to invade C. acetobutylicum pole to pole. Correlative fluorescence transmission electron microscopy demonstrated large-scale exchange of proteins. Flow cytometry analysis captured the extent and dynamic persistence of these interactions. Dividing hybrid cells were identified containing stained proteins from both organisms, thus demonstrating persistence of cells with exchanged cellular components. Fluorescence microscopy and flow cytometry of one species with stained RNA and the other tagged with a fluorescent protein demonstrated extensive RNA exchange and identified hybrid cells, some of which continued to divide, while some were in an advanced C. acetobutylicum sporulation form. These data demonstrate that cell fusion enables large-scale cellular material exchange between the two organisms. Although unanticipated and never previously reported, these phenomena are likely widely distributed in nature, have profound implications for species evolution and the function of microbial communities, and could find utility in biotechnology. They may shed new light onto little-understood phenomena, such as antibiotic heteroresistance of pathogens, pathogen invasion of human tissues, and the evolutionary trajectory and persistence of unculturable bacteria. IMPORTANCE We report that two different bacterial organisms engage in heterologous cell fusion that leads to massive exchange of cellular material, including proteins and RNA, and the formation of persistent hybrid cells. The interspecies cell fusion observed here involves a syntrophic microbial system, but these heterologous cell fusions were observed even under nonstrict syntrophic conditions, leaving open the possibility that strict syntrophy may not be necessary for interspecies cell fusion and cellular material exchange. Formation of hybrid cells that contain proteins and RNA from both organisms is unexpected and unprecedented. Such fusion events are likely widely distributed in nature, but have gone undetected. The implications are profound and may shed light onto many unexplained phenomena in human health, natural environments, evolutionary biology, and biotechnology.Kamil CharubinShannon ModlaJeffrey L. CaplanEleftherios Terry PapoutsakisAmerican Society for MicrobiologyarticleClostridium ljungdahliiClostridium acetobutylicumsyntrophyheterologous cell fusionhybrid cellsprotein exchangeMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution DOAJ
collection DOAJ
language EN
topic Clostridium ljungdahlii
Clostridium acetobutylicum
syntrophy
heterologous cell fusion
hybrid cells
protein exchange
Microbiology
QR1-502
spellingShingle Clostridium ljungdahlii
Clostridium acetobutylicum
syntrophy
heterologous cell fusion
hybrid cells
protein exchange
Microbiology
QR1-502
Kamil Charubin
Shannon Modla
Jeffrey L. Caplan
Eleftherios Terry Papoutsakis
Interspecies Microbial Fusion and Large-Scale Exchange of Cytoplasmic Proteins and RNA in a Syntrophic <italic toggle="yes">Clostridium</italic> Coculture
description ABSTRACT Microbial syntrophy is universal in nature, profoundly affecting the composition and function of microbiomes. We have recently reported data suggesting direct cell-to-cell interactions leading to electron and material exchange between the two microbes in the syntrophy between Clostridium ljungdahlii and C. acetobutylicum. Here, transmission electron microscopy and electron tomography demonstrated cell wall and membrane fusions between the two organisms, whereby C. ljungdahlii appears to invade C. acetobutylicum pole to pole. Correlative fluorescence transmission electron microscopy demonstrated large-scale exchange of proteins. Flow cytometry analysis captured the extent and dynamic persistence of these interactions. Dividing hybrid cells were identified containing stained proteins from both organisms, thus demonstrating persistence of cells with exchanged cellular components. Fluorescence microscopy and flow cytometry of one species with stained RNA and the other tagged with a fluorescent protein demonstrated extensive RNA exchange and identified hybrid cells, some of which continued to divide, while some were in an advanced C. acetobutylicum sporulation form. These data demonstrate that cell fusion enables large-scale cellular material exchange between the two organisms. Although unanticipated and never previously reported, these phenomena are likely widely distributed in nature, have profound implications for species evolution and the function of microbial communities, and could find utility in biotechnology. They may shed new light onto little-understood phenomena, such as antibiotic heteroresistance of pathogens, pathogen invasion of human tissues, and the evolutionary trajectory and persistence of unculturable bacteria. IMPORTANCE We report that two different bacterial organisms engage in heterologous cell fusion that leads to massive exchange of cellular material, including proteins and RNA, and the formation of persistent hybrid cells. The interspecies cell fusion observed here involves a syntrophic microbial system, but these heterologous cell fusions were observed even under nonstrict syntrophic conditions, leaving open the possibility that strict syntrophy may not be necessary for interspecies cell fusion and cellular material exchange. Formation of hybrid cells that contain proteins and RNA from both organisms is unexpected and unprecedented. Such fusion events are likely widely distributed in nature, but have gone undetected. The implications are profound and may shed light onto many unexplained phenomena in human health, natural environments, evolutionary biology, and biotechnology.
format article
author Kamil Charubin
Shannon Modla
Jeffrey L. Caplan
Eleftherios Terry Papoutsakis
author_facet Kamil Charubin
Shannon Modla
Jeffrey L. Caplan
Eleftherios Terry Papoutsakis
author_sort Kamil Charubin
title Interspecies Microbial Fusion and Large-Scale Exchange of Cytoplasmic Proteins and RNA in a Syntrophic <italic toggle="yes">Clostridium</italic> Coculture
title_short Interspecies Microbial Fusion and Large-Scale Exchange of Cytoplasmic Proteins and RNA in a Syntrophic <italic toggle="yes">Clostridium</italic> Coculture
title_full Interspecies Microbial Fusion and Large-Scale Exchange of Cytoplasmic Proteins and RNA in a Syntrophic <italic toggle="yes">Clostridium</italic> Coculture
title_fullStr Interspecies Microbial Fusion and Large-Scale Exchange of Cytoplasmic Proteins and RNA in a Syntrophic <italic toggle="yes">Clostridium</italic> Coculture
title_full_unstemmed Interspecies Microbial Fusion and Large-Scale Exchange of Cytoplasmic Proteins and RNA in a Syntrophic <italic toggle="yes">Clostridium</italic> Coculture
title_sort interspecies microbial fusion and large-scale exchange of cytoplasmic proteins and rna in a syntrophic <italic toggle="yes">clostridium</italic> coculture
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/ffc00ad7c5994fcb97d7b07713c744e4
work_keys_str_mv AT kamilcharubin interspeciesmicrobialfusionandlargescaleexchangeofcytoplasmicproteinsandrnainasyntrophicitalictoggleyesclostridiumitaliccoculture
AT shannonmodla interspeciesmicrobialfusionandlargescaleexchangeofcytoplasmicproteinsandrnainasyntrophicitalictoggleyesclostridiumitaliccoculture
AT jeffreylcaplan interspeciesmicrobialfusionandlargescaleexchangeofcytoplasmicproteinsandrnainasyntrophicitalictoggleyesclostridiumitaliccoculture
AT eleftheriosterrypapoutsakis interspeciesmicrobialfusionandlargescaleexchangeofcytoplasmicproteinsandrnainasyntrophicitalictoggleyesclostridiumitaliccoculture
_version_ 1718426945865121792