Microbial occurrence and symbiont detection in a global sample of lichen metagenomes

Autores
Tagirdzhanova, Gulnara; Saary, Paul; Cameron, Ellen S.; Allen, Carmen C. G.; Garber, Arkadiy I.; Escandón, David Díaz; Cook, Andrew T.; Goyette, Spencer; Nogerius, Veera Tuovinen; Passo, Alfredo; Mayrhofer, Helmut; Holien, Håkon; Tønsberg, Tor; Stein, Lisa Y.; Finn, Robert D.; Spribille, Toby
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
In lichen research, metagenomes are increasingly being used for evaluating symbiont composition and metabolic potential, but the overall content and limitations of these metagenomes have not been assessed. We reassembled over 400 publicly available metagenomes, generated metagenome-assembled genomes (MAGs), constructed phylogenomic trees, and mapped MAG occurrence and frequency across the data set. Ninety-seven percent of the 1,000 recovered MAGs were bacterial or the fungal symbiont that provides most cellular mass. Our mapping of recovered MAGs provides the most detailed survey to date of bacteria in lichens and shows that 4 family-level lineages from 2 phyla accounted for as many bacterial occurrences in lichens as all other 71 families from 16 phyla combined. Annotation of highly complete bacterial, fungal, and algal MAGs reveals functional profiles that suggest interdigitated vitamin prototrophies and auxotrophies, with most lichen fungi auxotrophic for biotin, most bacteria auxotrophic for thiamine and the few annotated algae with partial or complete pathways for both, suggesting a novel dimension of microbial cross-feeding in lichen symbioses. Contrary to longstanding hypotheses, we found no annotations consistent with nitrogen fixation in bacteria other than known cyanobacterial symbionts. Core lichen symbionts such as algae were recovered as MAGs in only a fraction of the lichen symbioses in which they are known to occur. However, the presence of these and other microbes could be detected at high frequency using small subunit rRNA analysis, including in many lichens in which they are not otherwise recognized to occur. The rate of MAG recovery correlates with sequencing depth, but is almost certainly influenced by biological attributes of organisms that affect the likelihood of DNA extraction, sequencing and successful assembly, including cellular abundance, ploidy and strain co-occurrence. Our results suggest that, though metagenomes are a powerful tool for surveying microbial occurrence, they are of limited use in assessing absence, and their interpretation should be guided by an awareness of the interacting effects of microbial community complexity and sequencing depth.
Fil: Tagirdzhanova, Gulnara. University of Alberta; Canadá
Fil: Saary, Paul. European Molecular Biology Laboratory. European Bioinformatics Institute.; Reino Unido
Fil: Cameron, Ellen S.. European Molecular Biology Laboratory. European Bioinformatics Institute.; Reino Unido
Fil: Allen, Carmen C. G.. University of Alberta; Canadá
Fil: Garber, Arkadiy I.. Arizona State University; Estados Unidos
Fil: Escandón, David Díaz. University of Alberta; Canadá
Fil: Cook, Andrew T.. University of Alberta; Canadá
Fil: Goyette, Spencer. University of Alberta; Canadá
Fil: Nogerius, Veera Tuovinen. Uppsala Universitet; Suecia
Fil: Passo, Alfredo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigaciones en Biodiversidad y Medioambiente. Universidad Nacional del Comahue. Centro Regional Universidad Bariloche. Instituto de Investigaciones en Biodiversidad y Medioambiente; Argentina
Fil: Mayrhofer, Helmut. University Of Graz.; Austria
Fil: Holien, Håkon. Nord University; Noruega
Fil: Tønsberg, Tor. University of Bergen; Noruega
Fil: Stein, Lisa Y.. University of Alberta; Canadá
Fil: Finn, Robert D.. European Molecular Biology Laboratory. European Bioinformatics Institute.; Reino Unido
Fil: Spribille, Toby. University of Alberta; Canadá
Materia
Lichens
Symbiosis
Bacteria
metagenomics
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/266905

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network_name_str CONICET Digital (CONICET)
spelling Microbial occurrence and symbiont detection in a global sample of lichen metagenomesTagirdzhanova, GulnaraSaary, PaulCameron, Ellen S.Allen, Carmen C. G.Garber, Arkadiy I.Escandón, David DíazCook, Andrew T.Goyette, SpencerNogerius, Veera TuovinenPasso, AlfredoMayrhofer, HelmutHolien, HåkonTønsberg, TorStein, Lisa Y.Finn, Robert D.Spribille, TobyLichensSymbiosisBacteriametagenomicshttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1In lichen research, metagenomes are increasingly being used for evaluating symbiont composition and metabolic potential, but the overall content and limitations of these metagenomes have not been assessed. We reassembled over 400 publicly available metagenomes, generated metagenome-assembled genomes (MAGs), constructed phylogenomic trees, and mapped MAG occurrence and frequency across the data set. Ninety-seven percent of the 1,000 recovered MAGs were bacterial or the fungal symbiont that provides most cellular mass. Our mapping of recovered MAGs provides the most detailed survey to date of bacteria in lichens and shows that 4 family-level lineages from 2 phyla accounted for as many bacterial occurrences in lichens as all other 71 families from 16 phyla combined. Annotation of highly complete bacterial, fungal, and algal MAGs reveals functional profiles that suggest interdigitated vitamin prototrophies and auxotrophies, with most lichen fungi auxotrophic for biotin, most bacteria auxotrophic for thiamine and the few annotated algae with partial or complete pathways for both, suggesting a novel dimension of microbial cross-feeding in lichen symbioses. Contrary to longstanding hypotheses, we found no annotations consistent with nitrogen fixation in bacteria other than known cyanobacterial symbionts. Core lichen symbionts such as algae were recovered as MAGs in only a fraction of the lichen symbioses in which they are known to occur. However, the presence of these and other microbes could be detected at high frequency using small subunit rRNA analysis, including in many lichens in which they are not otherwise recognized to occur. The rate of MAG recovery correlates with sequencing depth, but is almost certainly influenced by biological attributes of organisms that affect the likelihood of DNA extraction, sequencing and successful assembly, including cellular abundance, ploidy and strain co-occurrence. Our results suggest that, though metagenomes are a powerful tool for surveying microbial occurrence, they are of limited use in assessing absence, and their interpretation should be guided by an awareness of the interacting effects of microbial community complexity and sequencing depth.Fil: Tagirdzhanova, Gulnara. University of Alberta; CanadáFil: Saary, Paul. European Molecular Biology Laboratory. European Bioinformatics Institute.; Reino UnidoFil: Cameron, Ellen S.. European Molecular Biology Laboratory. European Bioinformatics Institute.; Reino UnidoFil: Allen, Carmen C. G.. University of Alberta; CanadáFil: Garber, Arkadiy I.. Arizona State University; Estados UnidosFil: Escandón, David Díaz. University of Alberta; CanadáFil: Cook, Andrew T.. University of Alberta; CanadáFil: Goyette, Spencer. University of Alberta; CanadáFil: Nogerius, Veera Tuovinen. Uppsala Universitet; SueciaFil: Passo, Alfredo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigaciones en Biodiversidad y Medioambiente. Universidad Nacional del Comahue. Centro Regional Universidad Bariloche. Instituto de Investigaciones en Biodiversidad y Medioambiente; ArgentinaFil: Mayrhofer, Helmut. University Of Graz.; AustriaFil: Holien, Håkon. Nord University; NoruegaFil: Tønsberg, Tor. University of Bergen; NoruegaFil: Stein, Lisa Y.. University of Alberta; CanadáFil: Finn, Robert D.. European Molecular Biology Laboratory. European Bioinformatics Institute.; Reino UnidoFil: Spribille, Toby. University of Alberta; CanadáPublic Library of Science2024-11info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/266905Tagirdzhanova, Gulnara; Saary, Paul; Cameron, Ellen S.; Allen, Carmen C. G.; Garber, Arkadiy I.; et al.; Microbial occurrence and symbiont detection in a global sample of lichen metagenomes; Public Library of Science; PLoS Biology; 22; 11; 11-2024; 1-421544-9173CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pbio.3002862info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-10T13:05:11Zoai:ri.conicet.gov.ar:11336/266905instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-10 13:05:11.474CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Microbial occurrence and symbiont detection in a global sample of lichen metagenomes
title Microbial occurrence and symbiont detection in a global sample of lichen metagenomes
spellingShingle Microbial occurrence and symbiont detection in a global sample of lichen metagenomes
Tagirdzhanova, Gulnara
Lichens
Symbiosis
Bacteria
metagenomics
title_short Microbial occurrence and symbiont detection in a global sample of lichen metagenomes
title_full Microbial occurrence and symbiont detection in a global sample of lichen metagenomes
title_fullStr Microbial occurrence and symbiont detection in a global sample of lichen metagenomes
title_full_unstemmed Microbial occurrence and symbiont detection in a global sample of lichen metagenomes
title_sort Microbial occurrence and symbiont detection in a global sample of lichen metagenomes
dc.creator.none.fl_str_mv Tagirdzhanova, Gulnara
Saary, Paul
Cameron, Ellen S.
Allen, Carmen C. G.
Garber, Arkadiy I.
Escandón, David Díaz
Cook, Andrew T.
Goyette, Spencer
Nogerius, Veera Tuovinen
Passo, Alfredo
Mayrhofer, Helmut
Holien, Håkon
Tønsberg, Tor
Stein, Lisa Y.
Finn, Robert D.
Spribille, Toby
author Tagirdzhanova, Gulnara
author_facet Tagirdzhanova, Gulnara
Saary, Paul
Cameron, Ellen S.
Allen, Carmen C. G.
Garber, Arkadiy I.
Escandón, David Díaz
Cook, Andrew T.
Goyette, Spencer
Nogerius, Veera Tuovinen
Passo, Alfredo
Mayrhofer, Helmut
Holien, Håkon
Tønsberg, Tor
Stein, Lisa Y.
Finn, Robert D.
Spribille, Toby
author_role author
author2 Saary, Paul
Cameron, Ellen S.
Allen, Carmen C. G.
Garber, Arkadiy I.
Escandón, David Díaz
Cook, Andrew T.
Goyette, Spencer
Nogerius, Veera Tuovinen
Passo, Alfredo
Mayrhofer, Helmut
Holien, Håkon
Tønsberg, Tor
Stein, Lisa Y.
Finn, Robert D.
Spribille, Toby
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Lichens
Symbiosis
Bacteria
metagenomics
topic Lichens
Symbiosis
Bacteria
metagenomics
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv In lichen research, metagenomes are increasingly being used for evaluating symbiont composition and metabolic potential, but the overall content and limitations of these metagenomes have not been assessed. We reassembled over 400 publicly available metagenomes, generated metagenome-assembled genomes (MAGs), constructed phylogenomic trees, and mapped MAG occurrence and frequency across the data set. Ninety-seven percent of the 1,000 recovered MAGs were bacterial or the fungal symbiont that provides most cellular mass. Our mapping of recovered MAGs provides the most detailed survey to date of bacteria in lichens and shows that 4 family-level lineages from 2 phyla accounted for as many bacterial occurrences in lichens as all other 71 families from 16 phyla combined. Annotation of highly complete bacterial, fungal, and algal MAGs reveals functional profiles that suggest interdigitated vitamin prototrophies and auxotrophies, with most lichen fungi auxotrophic for biotin, most bacteria auxotrophic for thiamine and the few annotated algae with partial or complete pathways for both, suggesting a novel dimension of microbial cross-feeding in lichen symbioses. Contrary to longstanding hypotheses, we found no annotations consistent with nitrogen fixation in bacteria other than known cyanobacterial symbionts. Core lichen symbionts such as algae were recovered as MAGs in only a fraction of the lichen symbioses in which they are known to occur. However, the presence of these and other microbes could be detected at high frequency using small subunit rRNA analysis, including in many lichens in which they are not otherwise recognized to occur. The rate of MAG recovery correlates with sequencing depth, but is almost certainly influenced by biological attributes of organisms that affect the likelihood of DNA extraction, sequencing and successful assembly, including cellular abundance, ploidy and strain co-occurrence. Our results suggest that, though metagenomes are a powerful tool for surveying microbial occurrence, they are of limited use in assessing absence, and their interpretation should be guided by an awareness of the interacting effects of microbial community complexity and sequencing depth.
Fil: Tagirdzhanova, Gulnara. University of Alberta; Canadá
Fil: Saary, Paul. European Molecular Biology Laboratory. European Bioinformatics Institute.; Reino Unido
Fil: Cameron, Ellen S.. European Molecular Biology Laboratory. European Bioinformatics Institute.; Reino Unido
Fil: Allen, Carmen C. G.. University of Alberta; Canadá
Fil: Garber, Arkadiy I.. Arizona State University; Estados Unidos
Fil: Escandón, David Díaz. University of Alberta; Canadá
Fil: Cook, Andrew T.. University of Alberta; Canadá
Fil: Goyette, Spencer. University of Alberta; Canadá
Fil: Nogerius, Veera Tuovinen. Uppsala Universitet; Suecia
Fil: Passo, Alfredo. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigaciones en Biodiversidad y Medioambiente. Universidad Nacional del Comahue. Centro Regional Universidad Bariloche. Instituto de Investigaciones en Biodiversidad y Medioambiente; Argentina
Fil: Mayrhofer, Helmut. University Of Graz.; Austria
Fil: Holien, Håkon. Nord University; Noruega
Fil: Tønsberg, Tor. University of Bergen; Noruega
Fil: Stein, Lisa Y.. University of Alberta; Canadá
Fil: Finn, Robert D.. European Molecular Biology Laboratory. European Bioinformatics Institute.; Reino Unido
Fil: Spribille, Toby. University of Alberta; Canadá
description In lichen research, metagenomes are increasingly being used for evaluating symbiont composition and metabolic potential, but the overall content and limitations of these metagenomes have not been assessed. We reassembled over 400 publicly available metagenomes, generated metagenome-assembled genomes (MAGs), constructed phylogenomic trees, and mapped MAG occurrence and frequency across the data set. Ninety-seven percent of the 1,000 recovered MAGs were bacterial or the fungal symbiont that provides most cellular mass. Our mapping of recovered MAGs provides the most detailed survey to date of bacteria in lichens and shows that 4 family-level lineages from 2 phyla accounted for as many bacterial occurrences in lichens as all other 71 families from 16 phyla combined. Annotation of highly complete bacterial, fungal, and algal MAGs reveals functional profiles that suggest interdigitated vitamin prototrophies and auxotrophies, with most lichen fungi auxotrophic for biotin, most bacteria auxotrophic for thiamine and the few annotated algae with partial or complete pathways for both, suggesting a novel dimension of microbial cross-feeding in lichen symbioses. Contrary to longstanding hypotheses, we found no annotations consistent with nitrogen fixation in bacteria other than known cyanobacterial symbionts. Core lichen symbionts such as algae were recovered as MAGs in only a fraction of the lichen symbioses in which they are known to occur. However, the presence of these and other microbes could be detected at high frequency using small subunit rRNA analysis, including in many lichens in which they are not otherwise recognized to occur. The rate of MAG recovery correlates with sequencing depth, but is almost certainly influenced by biological attributes of organisms that affect the likelihood of DNA extraction, sequencing and successful assembly, including cellular abundance, ploidy and strain co-occurrence. Our results suggest that, though metagenomes are a powerful tool for surveying microbial occurrence, they are of limited use in assessing absence, and their interpretation should be guided by an awareness of the interacting effects of microbial community complexity and sequencing depth.
publishDate 2024
dc.date.none.fl_str_mv 2024-11
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/266905
Tagirdzhanova, Gulnara; Saary, Paul; Cameron, Ellen S.; Allen, Carmen C. G.; Garber, Arkadiy I.; et al.; Microbial occurrence and symbiont detection in a global sample of lichen metagenomes; Public Library of Science; PLoS Biology; 22; 11; 11-2024; 1-42
1544-9173
CONICET Digital
CONICET
url http://hdl.handle.net/11336/266905
identifier_str_mv Tagirdzhanova, Gulnara; Saary, Paul; Cameron, Ellen S.; Allen, Carmen C. G.; Garber, Arkadiy I.; et al.; Microbial occurrence and symbiont detection in a global sample of lichen metagenomes; Public Library of Science; PLoS Biology; 22; 11; 11-2024; 1-42
1544-9173
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pbio.3002862
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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