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...

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Autores principales:	Kamil Charubin, Shannon Modla, Jeffrey L. Caplan, Eleftherios Terry Papoutsakis
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Clostridium ljungdahlii Clostridium acetobutylicum syntrophy heterologous cell fusion hybrid cells protein exchange Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ffc00ad7c5994fcb97d7b07713c744e4
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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
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Interspecies Microbial Fusion and Large-Scale Exchange of Cytoplasmic Proteins and RNA in a Syntrophic <italic toggle="yes">Clostridium</italic> Coculture

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