The microbiome as a biosensor: functional profiles elucidate hidden stress in hosts

Abstract Background Microbial communities are highly responsive to environmental cues, and both their structure and activity can be altered in response to changing conditions. We hypothesized that host-associated microbial communities, particularly those colonizing host surfaces, can serve as in situ sensors to reveal environmental conditions experienced by both microorganisms and the host. For a proof-of-concept, we studied a model plant-soil system and employed a non-deterministic gene-centric approach. A holistic analysis was performed using plants of two species and irrigation with water of low quality to induce host stress. Our analyses examined the genetic potential (DNA) and gene expression patterns (RNA) of plant-associated microbial communities, as well as transcriptional profiling of host plants. Results Transcriptional analysis of plants irrigated with treated wastewater revealed significant enrichment of general stress-associated root transcripts relative to plants irrigated with fresh water. Metagenomic analysis of root-associated microbial communities in treated wastewater-irrigated plants, however, revealed enrichment of more specific stress-associated genes relating to high levels of salt, high pH and lower levels of oxygen. Meta-analysis of these differentially abundant genes obtained from other metagenome studies, provided evidence of the link between environmental factors such as pH and oxygen and these genes. Analysis of microbial transcriptional response demonstrated that enriched gene content was actively expressed, which implies contemporary response to elevated levels of pH and salt. Conclusions We demonstrate here that microbial profiling can elucidate stress signals that cannot be observed even through interrogation of host transcriptome, leading to an alternate mechanism for evaluating in situ conditions experienced by host organisms. This study is a proof-of-concept for the use of microbial communities as microsensors, with great potential for interrogation of a wide range of host systems. Video Abstract Ausführliche Beschreibung

Gespeichert in:

Autor*in:	Avihai Zolti [verfasserIn] Stefan J. Green [verfasserIn] Noa Sela [verfasserIn] Yitzhak Hadar [verfasserIn] Dror Minz [verfasserIn]

Format:	E-Artikel
Sprache:	Englisch

Erschienen:	2020

Schlagwörter:	Microbiome Plant microbe interaction Host microbe interaction Biosensor

Übergeordnetes Werk:	In: Microbiome - BMC, 2013, 8(2020), 1, Seite 18
Übergeordnetes Werk:	volume:8 ; year:2020 ; number:1 ; pages:18

Links:	Link aufrufen Link aufrufen Link aufrufen Journal toc

DOI / URN:	10.1186/s40168-020-00850-9

Katalog-ID:	DOAJ043415466

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allfields_unstemmed	10.1186/s40168-020-00850-9 doi (DE-627)DOAJ043415466 (DE-599)DOAJe3af8fd8d792495fa1633af5b8aff26b DE-627 ger DE-627 rakwb eng QR100-130 Avihai Zolti verfasserin aut The microbiome as a biosensor: functional profiles elucidate hidden stress in hosts 2020 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Abstract Background Microbial communities are highly responsive to environmental cues, and both their structure and activity can be altered in response to changing conditions. We hypothesized that host-associated microbial communities, particularly those colonizing host surfaces, can serve as in situ sensors to reveal environmental conditions experienced by both microorganisms and the host. For a proof-of-concept, we studied a model plant-soil system and employed a non-deterministic gene-centric approach. A holistic analysis was performed using plants of two species and irrigation with water of low quality to induce host stress. Our analyses examined the genetic potential (DNA) and gene expression patterns (RNA) of plant-associated microbial communities, as well as transcriptional profiling of host plants. Results Transcriptional analysis of plants irrigated with treated wastewater revealed significant enrichment of general stress-associated root transcripts relative to plants irrigated with fresh water. Metagenomic analysis of root-associated microbial communities in treated wastewater-irrigated plants, however, revealed enrichment of more specific stress-associated genes relating to high levels of salt, high pH and lower levels of oxygen. Meta-analysis of these differentially abundant genes obtained from other metagenome studies, provided evidence of the link between environmental factors such as pH and oxygen and these genes. Analysis of microbial transcriptional response demonstrated that enriched gene content was actively expressed, which implies contemporary response to elevated levels of pH and salt. Conclusions We demonstrate here that microbial profiling can elucidate stress signals that cannot be observed even through interrogation of host transcriptome, leading to an alternate mechanism for evaluating in situ conditions experienced by host organisms. This study is a proof-of-concept for the use of microbial communities as microsensors, with great potential for interrogation of a wide range of host systems. Video Abstract Microbiome Plant microbe interaction Host microbe interaction Biosensor Microbial ecology Stefan J. Green verfasserin aut Noa Sela verfasserin aut Yitzhak Hadar verfasserin aut Dror Minz verfasserin aut In Microbiome BMC, 2013 8(2020), 1, Seite 18 (DE-627)734146140 (DE-600)2697425-3 20492618 nnns volume:8 year:2020 number:1 pages:18 https://doi.org/10.1186/s40168-020-00850-9 kostenfrei https://doaj.org/article/e3af8fd8d792495fa1633af5b8aff26b kostenfrei http://link.springer.com/article/10.1186/s40168-020-00850-9 kostenfrei https://doaj.org/toc/2049-2618 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 8 2020 1 18
allfieldsGer	10.1186/s40168-020-00850-9 doi (DE-627)DOAJ043415466 (DE-599)DOAJe3af8fd8d792495fa1633af5b8aff26b DE-627 ger DE-627 rakwb eng QR100-130 Avihai Zolti verfasserin aut The microbiome as a biosensor: functional profiles elucidate hidden stress in hosts 2020 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Abstract Background Microbial communities are highly responsive to environmental cues, and both their structure and activity can be altered in response to changing conditions. We hypothesized that host-associated microbial communities, particularly those colonizing host surfaces, can serve as in situ sensors to reveal environmental conditions experienced by both microorganisms and the host. For a proof-of-concept, we studied a model plant-soil system and employed a non-deterministic gene-centric approach. A holistic analysis was performed using plants of two species and irrigation with water of low quality to induce host stress. Our analyses examined the genetic potential (DNA) and gene expression patterns (RNA) of plant-associated microbial communities, as well as transcriptional profiling of host plants. Results Transcriptional analysis of plants irrigated with treated wastewater revealed significant enrichment of general stress-associated root transcripts relative to plants irrigated with fresh water. Metagenomic analysis of root-associated microbial communities in treated wastewater-irrigated plants, however, revealed enrichment of more specific stress-associated genes relating to high levels of salt, high pH and lower levels of oxygen. Meta-analysis of these differentially abundant genes obtained from other metagenome studies, provided evidence of the link between environmental factors such as pH and oxygen and these genes. Analysis of microbial transcriptional response demonstrated that enriched gene content was actively expressed, which implies contemporary response to elevated levels of pH and salt. Conclusions We demonstrate here that microbial profiling can elucidate stress signals that cannot be observed even through interrogation of host transcriptome, leading to an alternate mechanism for evaluating in situ conditions experienced by host organisms. This study is a proof-of-concept for the use of microbial communities as microsensors, with great potential for interrogation of a wide range of host systems. Video Abstract Microbiome Plant microbe interaction Host microbe interaction Biosensor Microbial ecology Stefan J. Green verfasserin aut Noa Sela verfasserin aut Yitzhak Hadar verfasserin aut Dror Minz verfasserin aut In Microbiome BMC, 2013 8(2020), 1, Seite 18 (DE-627)734146140 (DE-600)2697425-3 20492618 nnns volume:8 year:2020 number:1 pages:18 https://doi.org/10.1186/s40168-020-00850-9 kostenfrei https://doaj.org/article/e3af8fd8d792495fa1633af5b8aff26b kostenfrei http://link.springer.com/article/10.1186/s40168-020-00850-9 kostenfrei https://doaj.org/toc/2049-2618 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 8 2020 1 18
allfieldsSound	10.1186/s40168-020-00850-9 doi (DE-627)DOAJ043415466 (DE-599)DOAJe3af8fd8d792495fa1633af5b8aff26b DE-627 ger DE-627 rakwb eng QR100-130 Avihai Zolti verfasserin aut The microbiome as a biosensor: functional profiles elucidate hidden stress in hosts 2020 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Abstract Background Microbial communities are highly responsive to environmental cues, and both their structure and activity can be altered in response to changing conditions. We hypothesized that host-associated microbial communities, particularly those colonizing host surfaces, can serve as in situ sensors to reveal environmental conditions experienced by both microorganisms and the host. For a proof-of-concept, we studied a model plant-soil system and employed a non-deterministic gene-centric approach. A holistic analysis was performed using plants of two species and irrigation with water of low quality to induce host stress. Our analyses examined the genetic potential (DNA) and gene expression patterns (RNA) of plant-associated microbial communities, as well as transcriptional profiling of host plants. Results Transcriptional analysis of plants irrigated with treated wastewater revealed significant enrichment of general stress-associated root transcripts relative to plants irrigated with fresh water. Metagenomic analysis of root-associated microbial communities in treated wastewater-irrigated plants, however, revealed enrichment of more specific stress-associated genes relating to high levels of salt, high pH and lower levels of oxygen. Meta-analysis of these differentially abundant genes obtained from other metagenome studies, provided evidence of the link between environmental factors such as pH and oxygen and these genes. Analysis of microbial transcriptional response demonstrated that enriched gene content was actively expressed, which implies contemporary response to elevated levels of pH and salt. Conclusions We demonstrate here that microbial profiling can elucidate stress signals that cannot be observed even through interrogation of host transcriptome, leading to an alternate mechanism for evaluating in situ conditions experienced by host organisms. This study is a proof-of-concept for the use of microbial communities as microsensors, with great potential for interrogation of a wide range of host systems. Video Abstract Microbiome Plant microbe interaction Host microbe interaction Biosensor Microbial ecology Stefan J. Green verfasserin aut Noa Sela verfasserin aut Yitzhak Hadar verfasserin aut Dror Minz verfasserin aut In Microbiome BMC, 2013 8(2020), 1, Seite 18 (DE-627)734146140 (DE-600)2697425-3 20492618 nnns volume:8 year:2020 number:1 pages:18 https://doi.org/10.1186/s40168-020-00850-9 kostenfrei https://doaj.org/article/e3af8fd8d792495fa1633af5b8aff26b kostenfrei http://link.springer.com/article/10.1186/s40168-020-00850-9 kostenfrei https://doaj.org/toc/2049-2618 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 8 2020 1 18
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Metagenomic analysis of root-associated microbial communities in treated wastewater-irrigated plants, however, revealed enrichment of more specific stress-associated genes relating to high levels of salt, high pH and lower levels of oxygen. Meta-analysis of these differentially abundant genes obtained from other metagenome studies, provided evidence of the link between environmental factors such as pH and oxygen and these genes. Analysis of microbial transcriptional response demonstrated that enriched gene content was actively expressed, which implies contemporary response to elevated levels of pH and salt. Conclusions We demonstrate here that microbial profiling can elucidate stress signals that cannot be observed even through interrogation of host transcriptome, leading to an alternate mechanism for evaluating in situ conditions experienced by host organisms. This study is a proof-of-concept for the use of microbial communities as microsensors, with great potential for interrogation of a wide range of host systems. Video Abstract</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">Microbiome</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">Plant microbe interaction</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">Host microbe interaction</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">Biosensor</subfield></datafield><datafield tag="653" ind1=" " ind2="0"><subfield code="a">Microbial ecology</subfield></datafield><datafield tag="700" ind1="0" ind2=" "><subfield code="a">Stefan J. 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callnumber-first	Q - Science
author	Avihai Zolti
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topic_title	QR100-130 The microbiome as a biosensor: functional profiles elucidate hidden stress in hosts Microbiome Plant microbe interaction Host microbe interaction Biosensor
topic	misc QR100-130 misc Microbiome misc Plant microbe interaction misc Host microbe interaction misc Biosensor misc Microbial ecology
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title	The microbiome as a biosensor: functional profiles elucidate hidden stress in hosts
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title_full	The microbiome as a biosensor: functional profiles elucidate hidden stress in hosts
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title_sort	microbiome as a biosensor: functional profiles elucidate hidden stress in hosts
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title_auth	The microbiome as a biosensor: functional profiles elucidate hidden stress in hosts
abstract	Abstract Background Microbial communities are highly responsive to environmental cues, and both their structure and activity can be altered in response to changing conditions. We hypothesized that host-associated microbial communities, particularly those colonizing host surfaces, can serve as in situ sensors to reveal environmental conditions experienced by both microorganisms and the host. For a proof-of-concept, we studied a model plant-soil system and employed a non-deterministic gene-centric approach. A holistic analysis was performed using plants of two species and irrigation with water of low quality to induce host stress. Our analyses examined the genetic potential (DNA) and gene expression patterns (RNA) of plant-associated microbial communities, as well as transcriptional profiling of host plants. Results Transcriptional analysis of plants irrigated with treated wastewater revealed significant enrichment of general stress-associated root transcripts relative to plants irrigated with fresh water. Metagenomic analysis of root-associated microbial communities in treated wastewater-irrigated plants, however, revealed enrichment of more specific stress-associated genes relating to high levels of salt, high pH and lower levels of oxygen. Meta-analysis of these differentially abundant genes obtained from other metagenome studies, provided evidence of the link between environmental factors such as pH and oxygen and these genes. Analysis of microbial transcriptional response demonstrated that enriched gene content was actively expressed, which implies contemporary response to elevated levels of pH and salt. Conclusions We demonstrate here that microbial profiling can elucidate stress signals that cannot be observed even through interrogation of host transcriptome, leading to an alternate mechanism for evaluating in situ conditions experienced by host organisms. This study is a proof-of-concept for the use of microbial communities as microsensors, with great potential for interrogation of a wide range of host systems. Video Abstract
abstractGer	Abstract Background Microbial communities are highly responsive to environmental cues, and both their structure and activity can be altered in response to changing conditions. We hypothesized that host-associated microbial communities, particularly those colonizing host surfaces, can serve as in situ sensors to reveal environmental conditions experienced by both microorganisms and the host. For a proof-of-concept, we studied a model plant-soil system and employed a non-deterministic gene-centric approach. A holistic analysis was performed using plants of two species and irrigation with water of low quality to induce host stress. Our analyses examined the genetic potential (DNA) and gene expression patterns (RNA) of plant-associated microbial communities, as well as transcriptional profiling of host plants. Results Transcriptional analysis of plants irrigated with treated wastewater revealed significant enrichment of general stress-associated root transcripts relative to plants irrigated with fresh water. Metagenomic analysis of root-associated microbial communities in treated wastewater-irrigated plants, however, revealed enrichment of more specific stress-associated genes relating to high levels of salt, high pH and lower levels of oxygen. Meta-analysis of these differentially abundant genes obtained from other metagenome studies, provided evidence of the link between environmental factors such as pH and oxygen and these genes. Analysis of microbial transcriptional response demonstrated that enriched gene content was actively expressed, which implies contemporary response to elevated levels of pH and salt. Conclusions We demonstrate here that microbial profiling can elucidate stress signals that cannot be observed even through interrogation of host transcriptome, leading to an alternate mechanism for evaluating in situ conditions experienced by host organisms. This study is a proof-of-concept for the use of microbial communities as microsensors, with great potential for interrogation of a wide range of host systems. Video Abstract
abstract_unstemmed	Abstract Background Microbial communities are highly responsive to environmental cues, and both their structure and activity can be altered in response to changing conditions. We hypothesized that host-associated microbial communities, particularly those colonizing host surfaces, can serve as in situ sensors to reveal environmental conditions experienced by both microorganisms and the host. For a proof-of-concept, we studied a model plant-soil system and employed a non-deterministic gene-centric approach. A holistic analysis was performed using plants of two species and irrigation with water of low quality to induce host stress. Our analyses examined the genetic potential (DNA) and gene expression patterns (RNA) of plant-associated microbial communities, as well as transcriptional profiling of host plants. Results Transcriptional analysis of plants irrigated with treated wastewater revealed significant enrichment of general stress-associated root transcripts relative to plants irrigated with fresh water. Metagenomic analysis of root-associated microbial communities in treated wastewater-irrigated plants, however, revealed enrichment of more specific stress-associated genes relating to high levels of salt, high pH and lower levels of oxygen. Meta-analysis of these differentially abundant genes obtained from other metagenome studies, provided evidence of the link between environmental factors such as pH and oxygen and these genes. Analysis of microbial transcriptional response demonstrated that enriched gene content was actively expressed, which implies contemporary response to elevated levels of pH and salt. Conclusions We demonstrate here that microbial profiling can elucidate stress signals that cannot be observed even through interrogation of host transcriptome, leading to an alternate mechanism for evaluating in situ conditions experienced by host organisms. This study is a proof-of-concept for the use of microbial communities as microsensors, with great potential for interrogation of a wide range of host systems. Video Abstract
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title_short	The microbiome as a biosensor: functional profiles elucidate hidden stress in hosts
url	https://doi.org/10.1186/s40168-020-00850-9 https://doaj.org/article/e3af8fd8d792495fa1633af5b8aff26b http://link.springer.com/article/10.1186/s40168-020-00850-9 https://doaj.org/toc/2049-2618
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up_date	2024-07-03T17:27:21.327Z
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Metagenomic analysis of root-associated microbial communities in treated wastewater-irrigated plants, however, revealed enrichment of more specific stress-associated genes relating to high levels of salt, high pH and lower levels of oxygen. Meta-analysis of these differentially abundant genes obtained from other metagenome studies, provided evidence of the link between environmental factors such as pH and oxygen and these genes. Analysis of microbial transcriptional response demonstrated that enriched gene content was actively expressed, which implies contemporary response to elevated levels of pH and salt. Conclusions We demonstrate here that microbial profiling can elucidate stress signals that cannot be observed even through interrogation of host transcriptome, leading to an alternate mechanism for evaluating in situ conditions experienced by host organisms. 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