Comparative single-cell genomics of two uncultivated Naegleria species harboring Legionella cobionts
Amoeboflagellates of the genus Naegleria are free-living protists ubiquitously found in soil and freshwater habitats worldwide. They include the "brain-eating amoeba" Naegleria fowleri, an opportunistic pathogen that causes primary amoebic meningoencephalitis, a rare but fatal infection of...
| Autores: | , , , , , , , , , , , |
|---|---|
| Formato: | artículo |
| Estado: | Versión publicada |
| Fecha de publicación: | 2025 |
| País: | España |
| Recursos: | Consejo Superior de Investigaciones Científicas (CSIC) |
| Repositorio: | DIGITAL.CSIC. Repositorio Institucional del CSIC |
| OAI Identifier: | oai:digital.csic.es:10261/418654 |
| Acesso em linha: | http://hdl.handle.net/10261/418654 https://api.elsevier.com/content/abstract/scopus_id/105017668385 |
| Access Level: | acceso abierto |
| Palavra-chave: | Heterolobosea Legionellaceae Amoeboflagellates Effectors Intracellular pathogens Protists Secretion systems |
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oai:digital.csic.es:10261/418654 |
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España |
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Comparative single-cell genomics of two uncultivated Naegleria species harboring Legionella cobionts |
| title |
Comparative single-cell genomics of two uncultivated Naegleria species harboring Legionella cobionts |
| spellingShingle |
Comparative single-cell genomics of two uncultivated Naegleria species harboring Legionella cobionts McGowan, Jamie Heterolobosea Legionellaceae Amoeboflagellates Effectors Intracellular pathogens Protists Secretion systems |
| title_short |
Comparative single-cell genomics of two uncultivated Naegleria species harboring Legionella cobionts |
| title_full |
Comparative single-cell genomics of two uncultivated Naegleria species harboring Legionella cobionts |
| title_fullStr |
Comparative single-cell genomics of two uncultivated Naegleria species harboring Legionella cobionts |
| title_full_unstemmed |
Comparative single-cell genomics of two uncultivated Naegleria species harboring Legionella cobionts |
| title_sort |
Comparative single-cell genomics of two uncultivated Naegleria species harboring Legionella cobionts |
| dc.creator.none.fl_str_mv |
McGowan, Jamie Kilias, Estelle S. Lipscombe, James Alacid, Elisabet Barker, Tom Catchpole, Leah McTaggart, Seanna Warring, Sally D. Gharbi, Karim Richards, Thomas A. Hall, Neil Swarbreck, David |
| author |
McGowan, Jamie |
| author_facet |
McGowan, Jamie Kilias, Estelle S. Lipscombe, James Alacid, Elisabet Barker, Tom Catchpole, Leah McTaggart, Seanna Warring, Sally D. Gharbi, Karim Richards, Thomas A. Hall, Neil Swarbreck, David |
| author_role |
author |
| author2 |
Kilias, Estelle S. Lipscombe, James Alacid, Elisabet Barker, Tom Catchpole, Leah McTaggart, Seanna Warring, Sally D. Gharbi, Karim Richards, Thomas A. Hall, Neil Swarbreck, David |
| author2_role |
author author author author author author author author author author author |
| dc.contributor.none.fl_str_mv |
Wellcome Trust Biotechnology and Biological Sciences Research Council (UK) Royal Society (UK) McGowan, Jamie [0000-0002-4240-5175] |
| dc.subject.none.fl_str_mv |
Heterolobosea Legionellaceae Amoeboflagellates Effectors Intracellular pathogens Protists Secretion systems |
| topic |
Heterolobosea Legionellaceae Amoeboflagellates Effectors Intracellular pathogens Protists Secretion systems |
| description |
Amoeboflagellates of the genus Naegleria are free-living protists ubiquitously found in soil and freshwater habitats worldwide. They include the "brain-eating amoeba" Naegleria fowleri, an opportunistic pathogen that causes primary amoebic meningoencephalitis, a rare but fatal infection of humans. Beyond their direct pathogenicity, protists can also act as environmental reservoirs for intracellular bacterial pathogens, such as Legionella spp., to persist and multiply in the environment. In this study, we carried out single-cell genome sequencing of two uncultivated Naegleria species isolated from the River Leam in England. From single cells, we generated two highly complete Naegleria genomes. Phylogenetic analyses placed these species as close relatives of Naegleria fultoni and Naegleria pagei. Exploring Naegleria evolutionary genomics, we identified gene families encoding antistasin-like domains, which have been characterized as factors that inhibit coagulation in blood-feeding leeches. Antistasin-like domains were identified in all sequenced Naegleria species and their close relative Willaertia magna, yet are otherwise largely restricted to animal genomes. Significantly, we recovered highly complete bacterial genomes from each Naegleria single-cell sample. Phylogenomic analysis revealed that both bacteria belong to the Legionellaceae family. Both bacterial genomes encode comprehensive sets of secretion systems and effector arsenals. We identified putative Legionella effectors that resemble TAL (Transcription activator-like) effectors from plant pathogenic Xanthomonas spp. in terms of protein sequence and predicted structure, representing a potentially novel class of Legionella effectors. Our study highlights the advantages of single-cell environmental genomics approaches, which enable direct association of intracellular pathogens with their hosts to better understand the evolution of host-pathogen interactions.IMPORTANCEBeyond their direct pathogenic potential, amoebae and other protists found in the environment can indirectly threaten human health by serving as reservoirs for intracellular bacterial pathogens to persist, evolve, and multiply in the environment. Despite their importance, protist-bacterial interactions remain poorly understood. In this study, we employed single-cell genomics to sequence the genomes of two uncultivated Naegleria amoebae, both harboring novel Legionella bacteria. From individual cells, we recovered highly complete eukaryotic and bacterial cobiont genome assemblies. Our work demonstrates the power of single-cell sequencing approaches in directly linking intracellular pathogens to their hosts to better understand the evolution of protist-bacterial interactions and the role that protists play in facilitating bacterial pathogens to persist long term in the environment. |
| publishDate |
2025 |
| dc.date.none.fl_str_mv |
2025 2026 2026 |
| dc.type.none.fl_str_mv |
info:eu-repo/semantics/article http://purl.org/coar/resource_type/c_6501 Publisher's version info:eu-repo/semantics/publishedVersion |
| format |
article |
| status_str |
publishedVersion |
| dc.identifier.none.fl_str_mv |
http://hdl.handle.net/10261/418654 https://api.elsevier.com/content/abstract/scopus_id/105017668385 |
| url |
http://hdl.handle.net/10261/418654 https://api.elsevier.com/content/abstract/scopus_id/105017668385 |
| dc.language.none.fl_str_mv |
Inglés |
| language_invalid_str_mv |
Inglés |
| dc.relation.none.fl_str_mv |
Naegleria environmental single-cell sequencing. https://www.ebi.ac.uk/ena/browser/view/PRJEB85689 McGowan, Jamie; Kilias, Estelle S.; Lipscombe, James; Alacid, Elisabet; Barker, Tom; Catchpole, Leah; McTaggart, Seanna; Warring, Sally D.; Gharbi, Karim; Richards, Thomas A.; Hall, Neil; Swarbreck, David; 2025; Comparative single-cell genomics of two uncultivated Naegleria species harbouring Legionella cobionts [Dataset]; Zenodo; https://doi.org/10.5281/zenodo.15721720 https://doi.org/10.1128/msphere.00352-25 No |
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info:eu-repo/semantics/openAccess |
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openAccess |
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application/pdf |
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American Society for Microbiology |
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American Society for Microbiology |
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reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC instname:Consejo Superior de Investigaciones Científicas (CSIC) |
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Consejo Superior de Investigaciones Científicas (CSIC) |
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DIGITAL.CSIC. Repositorio Institucional del CSIC |
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DIGITAL.CSIC. Repositorio Institucional del CSIC |
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1869425803799822336 |
| spelling |
Comparative single-cell genomics of two uncultivated Naegleria species harboring Legionella cobiontsMcGowan, JamieKilias, Estelle S.Lipscombe, JamesAlacid, ElisabetBarker, TomCatchpole, LeahMcTaggart, SeannaWarring, Sally D.Gharbi, KarimRichards, Thomas A.Hall, NeilSwarbreck, DavidHeteroloboseaLegionellaceaeAmoeboflagellatesEffectorsIntracellular pathogensProtistsSecretion systemsAmoeboflagellates of the genus Naegleria are free-living protists ubiquitously found in soil and freshwater habitats worldwide. They include the "brain-eating amoeba" Naegleria fowleri, an opportunistic pathogen that causes primary amoebic meningoencephalitis, a rare but fatal infection of humans. Beyond their direct pathogenicity, protists can also act as environmental reservoirs for intracellular bacterial pathogens, such as Legionella spp., to persist and multiply in the environment. In this study, we carried out single-cell genome sequencing of two uncultivated Naegleria species isolated from the River Leam in England. From single cells, we generated two highly complete Naegleria genomes. Phylogenetic analyses placed these species as close relatives of Naegleria fultoni and Naegleria pagei. Exploring Naegleria evolutionary genomics, we identified gene families encoding antistasin-like domains, which have been characterized as factors that inhibit coagulation in blood-feeding leeches. Antistasin-like domains were identified in all sequenced Naegleria species and their close relative Willaertia magna, yet are otherwise largely restricted to animal genomes. Significantly, we recovered highly complete bacterial genomes from each Naegleria single-cell sample. Phylogenomic analysis revealed that both bacteria belong to the Legionellaceae family. Both bacterial genomes encode comprehensive sets of secretion systems and effector arsenals. We identified putative Legionella effectors that resemble TAL (Transcription activator-like) effectors from plant pathogenic Xanthomonas spp. in terms of protein sequence and predicted structure, representing a potentially novel class of Legionella effectors. Our study highlights the advantages of single-cell environmental genomics approaches, which enable direct association of intracellular pathogens with their hosts to better understand the evolution of host-pathogen interactions.IMPORTANCEBeyond their direct pathogenic potential, amoebae and other protists found in the environment can indirectly threaten human health by serving as reservoirs for intracellular bacterial pathogens to persist, evolve, and multiply in the environment. Despite their importance, protist-bacterial interactions remain poorly understood. In this study, we employed single-cell genomics to sequence the genomes of two uncultivated Naegleria amoebae, both harboring novel Legionella bacteria. From individual cells, we recovered highly complete eukaryotic and bacterial cobiont genome assemblies. Our work demonstrates the power of single-cell sequencing approaches in directly linking intracellular pathogens to their hosts to better understand the evolution of protist-bacterial interactions and the role that protists play in facilitating bacterial pathogens to persist long term in the environment.We would like to acknowledge the members of the Technical Genomics Group at the Earlham Institute and note the specific contributions of Chris Watkins, Sacha Lucchini, Kendall Baker, and Neil Shearer. We also acknowledge the work delivered via the Research Computing Group at the Earlham Institute who manages and delivers High-Performance Computing. This work was funded by the Wellcome Trust Darwin Tree of Life Awards (218328 and 226458) and by the Biotechnology and Biological Sciences Research Council (BBSRC), part of UK Research and Innovation, through the Core Capability Grant (BB/CCG2220/1) at the Earlham Institute; the Earlham Institute Strategic Program Grant Decoding Biodiversity (BBX011089/1) and its constituent work packages (BBS/E/ER/230002A and BBS/E/ER/230002B). T.A.R. is supported by a Royal Society University Research Fellowship (URF/R/191005).Peer reviewedAmerican Society for MicrobiologyWellcome TrustBiotechnology and Biological Sciences Research Council (UK)Royal Society (UK)McGowan, Jamie [0000-0002-4240-5175]202620262025info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/418654https://api.elsevier.com/content/abstract/scopus_id/105017668385reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésNaegleria environmental single-cell sequencing. https://www.ebi.ac.uk/ena/browser/view/PRJEB85689McGowan, Jamie; Kilias, Estelle S.; Lipscombe, James; Alacid, Elisabet; Barker, Tom; Catchpole, Leah; McTaggart, Seanna; Warring, Sally D.; Gharbi, Karim; Richards, Thomas A.; Hall, Neil; Swarbreck, David; 2025; Comparative single-cell genomics of two uncultivated Naegleria species harbouring Legionella cobionts [Dataset]; Zenodo; https://doi.org/10.5281/zenodo.15721720https://doi.org/10.1128/msphere.00352-25Noinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/4186542026-05-22T06:33:51Z |
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15,811543 |