Molecular Dialogues between Early Divergent Fungi and Bacteria in an Antagonism versus a Mutualism

ABSTRACT Fungal-bacterial symbioses range from antagonisms to mutualisms and remain one of the least understood interdomain interactions despite their ubiquity as well as ecological and medical importance. To build a predictive conceptual framework for understanding interactions between fungi and ba...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Olga A. Lastovetsky, Lev D. Krasnovsky, Xiaotian Qin, Maria L. Gaspar, Andrii P. Gryganskyi, Marcel Huntemann, Alicia Clum, Manoj Pillay, Krishnaveni Palaniappan, Neha Varghese, Natalia Mikhailova, Dimitrios Stamatis, T. B. K. Reddy, Chris Daum, Nicole Shapiro, Natalia Ivanova, Nikos Kyrpides, Tanja Woyke, Teresa E. Pawlowska
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	cell wall remodeling innate immunity Mycetohabitans reactive oxygen species Rhizopus microsporus Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/311bcffde26749ddaddf1fb3e086628b
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:311bcffde26749ddaddf1fb3e086628b
record_format	dspace
spelling	oai:doaj.org-article:311bcffde26749ddaddf1fb3e086628b2021-11-15T16:19:09ZMolecular Dialogues between Early Divergent Fungi and Bacteria in an Antagonism versus a Mutualism10.1128/mBio.02088-202150-7511https://doaj.org/article/311bcffde26749ddaddf1fb3e086628b2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02088-20https://doaj.org/toc/2150-7511ABSTRACT Fungal-bacterial symbioses range from antagonisms to mutualisms and remain one of the least understood interdomain interactions despite their ubiquity as well as ecological and medical importance. To build a predictive conceptual framework for understanding interactions between fungi and bacteria in different types of symbioses, we surveyed fungal and bacterial transcriptional responses in the mutualism between Rhizopus microsporus (Rm) (ATCC 52813, host) and its Mycetohabitans (formerly Burkholderia) endobacteria versus the antagonism between a nonhost Rm (ATCC 11559) and Mycetohabitans isolated from the host, at two time points, before and after partner physical contact. We found that bacteria and fungi sensed each other before contact and altered gene expression patterns accordingly. Mycetohabitans did not discriminate between the host and nonhost and engaged a common set of genes encoding known as well as novel symbiosis factors. In contrast, responses of the host versus nonhost to endobacteria were dramatically different, converging on the altered expression of genes involved in cell wall biosynthesis and reactive oxygen species (ROS) metabolism. On the basis of the observed patterns, we formulated a set of hypotheses describing fungal-bacterial interactions and tested some of them. By conducting ROS measurements, we confirmed that nonhost fungi increased production of ROS in response to endobacteria, whereas host fungi quenched their ROS output, suggesting that ROS metabolism contributes to the nonhost resistance to bacterial infection and the host ability to form a mutualism. Overall, our study offers a testable framework of predictions describing interactions of early divergent Mucoromycotina fungi with bacteria. IMPORTANCE Animals and plants interact with microbes by engaging specific surveillance systems, regulatory networks, and response modules that allow for accommodation of mutualists and defense against antagonists. Antimicrobial defense responses are mediated in both animals and plants by innate immunity systems that owe their functional similarities to convergent evolution. Like animals and plants, fungi interact with bacteria. However, the principles governing these relations are only now being discovered. In a study system of host and nonhost fungi interacting with a bacterium isolated from the host, we found that bacteria used a common gene repertoire to engage both partners. In contrast, fungal responses to bacteria differed dramatically between the host and nonhost. These findings suggest that as in animals and plants, the genetic makeup of the fungus determines whether bacterial partners are perceived as mutualists or antagonists and what specific regulatory networks and response modules are initiated during each encounter.Olga A. LastovetskyLev D. KrasnovskyXiaotian QinMaria L. GasparAndrii P. GryganskyiMarcel HuntemannAlicia ClumManoj PillayKrishnaveni PalaniappanNeha VargheseNatalia MikhailovaDimitrios StamatisT. B. K. ReddyChris DaumNicole ShapiroNatalia IvanovaNikos KyrpidesTanja WoykeTeresa E. PawlowskaAmerican Society for Microbiologyarticlecell wall remodelinginnate immunityMycetohabitansreactive oxygen speciesRhizopus microsporuscell wall remodelingMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	cell wall remodeling innate immunity Mycetohabitans reactive oxygen species Rhizopus microsporus cell wall remodeling Microbiology QR1-502
spellingShingle	cell wall remodeling innate immunity Mycetohabitans reactive oxygen species Rhizopus microsporus cell wall remodeling Microbiology QR1-502 Olga A. Lastovetsky Lev D. Krasnovsky Xiaotian Qin Maria L. Gaspar Andrii P. Gryganskyi Marcel Huntemann Alicia Clum Manoj Pillay Krishnaveni Palaniappan Neha Varghese Natalia Mikhailova Dimitrios Stamatis T. B. K. Reddy Chris Daum Nicole Shapiro Natalia Ivanova Nikos Kyrpides Tanja Woyke Teresa E. Pawlowska Molecular Dialogues between Early Divergent Fungi and Bacteria in an Antagonism versus a Mutualism
description	ABSTRACT Fungal-bacterial symbioses range from antagonisms to mutualisms and remain one of the least understood interdomain interactions despite their ubiquity as well as ecological and medical importance. To build a predictive conceptual framework for understanding interactions between fungi and bacteria in different types of symbioses, we surveyed fungal and bacterial transcriptional responses in the mutualism between Rhizopus microsporus (Rm) (ATCC 52813, host) and its Mycetohabitans (formerly Burkholderia) endobacteria versus the antagonism between a nonhost Rm (ATCC 11559) and Mycetohabitans isolated from the host, at two time points, before and after partner physical contact. We found that bacteria and fungi sensed each other before contact and altered gene expression patterns accordingly. Mycetohabitans did not discriminate between the host and nonhost and engaged a common set of genes encoding known as well as novel symbiosis factors. In contrast, responses of the host versus nonhost to endobacteria were dramatically different, converging on the altered expression of genes involved in cell wall biosynthesis and reactive oxygen species (ROS) metabolism. On the basis of the observed patterns, we formulated a set of hypotheses describing fungal-bacterial interactions and tested some of them. By conducting ROS measurements, we confirmed that nonhost fungi increased production of ROS in response to endobacteria, whereas host fungi quenched their ROS output, suggesting that ROS metabolism contributes to the nonhost resistance to bacterial infection and the host ability to form a mutualism. Overall, our study offers a testable framework of predictions describing interactions of early divergent Mucoromycotina fungi with bacteria. IMPORTANCE Animals and plants interact with microbes by engaging specific surveillance systems, regulatory networks, and response modules that allow for accommodation of mutualists and defense against antagonists. Antimicrobial defense responses are mediated in both animals and plants by innate immunity systems that owe their functional similarities to convergent evolution. Like animals and plants, fungi interact with bacteria. However, the principles governing these relations are only now being discovered. In a study system of host and nonhost fungi interacting with a bacterium isolated from the host, we found that bacteria used a common gene repertoire to engage both partners. In contrast, fungal responses to bacteria differed dramatically between the host and nonhost. These findings suggest that as in animals and plants, the genetic makeup of the fungus determines whether bacterial partners are perceived as mutualists or antagonists and what specific regulatory networks and response modules are initiated during each encounter.
format	article
author	Olga A. Lastovetsky Lev D. Krasnovsky Xiaotian Qin Maria L. Gaspar Andrii P. Gryganskyi Marcel Huntemann Alicia Clum Manoj Pillay Krishnaveni Palaniappan Neha Varghese Natalia Mikhailova Dimitrios Stamatis T. B. K. Reddy Chris Daum Nicole Shapiro Natalia Ivanova Nikos Kyrpides Tanja Woyke Teresa E. Pawlowska
author_facet	Olga A. Lastovetsky Lev D. Krasnovsky Xiaotian Qin Maria L. Gaspar Andrii P. Gryganskyi Marcel Huntemann Alicia Clum Manoj Pillay Krishnaveni Palaniappan Neha Varghese Natalia Mikhailova Dimitrios Stamatis T. B. K. Reddy Chris Daum Nicole Shapiro Natalia Ivanova Nikos Kyrpides Tanja Woyke Teresa E. Pawlowska
author_sort	Olga A. Lastovetsky
title	Molecular Dialogues between Early Divergent Fungi and Bacteria in an Antagonism versus a Mutualism
title_short	Molecular Dialogues between Early Divergent Fungi and Bacteria in an Antagonism versus a Mutualism
title_full	Molecular Dialogues between Early Divergent Fungi and Bacteria in an Antagonism versus a Mutualism
title_fullStr	Molecular Dialogues between Early Divergent Fungi and Bacteria in an Antagonism versus a Mutualism
title_full_unstemmed	Molecular Dialogues between Early Divergent Fungi and Bacteria in an Antagonism versus a Mutualism
title_sort	molecular dialogues between early divergent fungi and bacteria in an antagonism versus a mutualism
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/311bcffde26749ddaddf1fb3e086628b
work_keys_str_mv	AT olgaalastovetsky moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT levdkrasnovsky moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT xiaotianqin moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT marialgaspar moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT andriipgryganskyi moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT marcelhuntemann moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT aliciaclum moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT manojpillay moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT krishnavenipalaniappan moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT nehavarghese moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT nataliamikhailova moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT dimitriosstamatis moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT tbkreddy moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT chrisdaum moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT nicoleshapiro moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT nataliaivanova moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT nikoskyrpides moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT tanjawoyke moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism AT teresaepawlowska moleculardialoguesbetweenearlydivergentfungiandbacteriainanantagonismversusamutualism
_version_	1718426894602338304

Molecular Dialogues between Early Divergent Fungi and Bacteria in an Antagonism versus a Mutualism

Ejemplares similares