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
- Institución
- Consejo Nacional de Investigaciones Científicas y Técnicas
- OAI Identificador
- oai:ri.conicet.gov.ar:11336/266905
Ver los metadatos del registro completo
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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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12.993085 |