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Single-cell genomics of a rare environmental alphaproteobacterium provides unique insights into Rickettsiaceae evolution
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
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2015 (English)In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 9, no 11, 2373-2385 p.Article in journal (Refereed) Published
Abstract [en]

The bacterial family Rickettsiaceae includes a group of well-known etiological agents of many human and vertebrate diseases, including epidemic typhus-causing pathogen Rickettsia prowazekii. Owing to their medical relevance, rickettsiae have attracted a great deal of attention and their host-pathogen interactions have been thoroughly investigated. All known members display obligate intracellular lifestyles, and the best-studied genera, Rickettsia and Orientia, include species that are hosted by terrestrial arthropods. Their obligate intracellular lifestyle and host adaptation is reflected in the small size of their genomes, a general feature shared with all other families of the Rickettsiales. Yet, despite that the Rickettsiaceae and other Rickettsiales families have been extensively studied for decades, many details of the origin and evolution of their obligate host-association remain elusive. Here we report the discovery and single-cell sequencing of 'Candidatus Arcanobacter lacustris', a rare environmental alphaproteobacterium that was sampled from Damariscotta Lake that represents a deeply rooting sister lineage of the Rickettsiaceae. Intriguingly, phylogenomic and comparative analysis of the partial 'Candidatus Arcanobacter lacustris' genome revealed the presence chemotaxis genes and vertically inherited flagellar genes, a novelty in sequenced Rickettsiaceae, as well as several host-associated features. This finding suggests that the ancestor of the Rickettsiaceae might have had a facultative intracellular lifestyle. Our study underlines the efficacy of single-cell genomics for studying microbial diversity and evolution in general, and for rare microbial cells in particular.

Place, publisher, year, edition, pages
2015. Vol. 9, no 11, 2373-2385 p.
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-267117DOI: 10.1038/ismej.2015.46ISI: 000365091700005PubMedID: 25848874OAI: oai:DiVA.org:uu-267117DiVA: diva2:872211
Funder
Swedish Research Council, 621-2009-4813Swedish Research Council, 621-2011-4669EU, European Research Council, 310039-PUZZLE_CELLEU, European Research Council, 281633-EvoChlamy
Available from: 2015-11-18 Created: 2015-11-18 Last updated: 2017-12-01Bibliographically approved
In thesis
1. Exploration of microbial diversity and evolution through cultivation independent phylogenomics
Open this publication in new window or tab >>Exploration of microbial diversity and evolution through cultivation independent phylogenomics
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Our understanding of microbial evolution is largely dependent on available genomic data of diverse organisms. Yet, genome-sequencing efforts have mostly ignored the diverse uncultivable majority in favor of cultivable and sociologically relevant organisms. In this thesis, I have applied and developed cultivation independent methods to explore microbial diversity and obtain genomic data in an unbiased manner. The obtained genomes were then used to study the evolution of mitochondria, Rickettsiales and Haloarchaea.

Metagenomic binning of oceanic samples recovered draft genomes for thirteen novel Alphaproteobacteria-related lineages. Phylogenomics analyses utilizing the improved taxon sample suggested that mitochondria are not related to Rickettsiales but rather evolved from a proteobacterial lineage closely related to all sampled alphaproteobacteria.

Single-cell genomics and metagenomics of lake and oceanic samples, respectively, identified previously unobserved Rickettsiales-related lineages. They branched early relative to characterized Rickettsiales and encoded flagellar genes, a feature once thought absent in this order. Flagella are most likely an ancestral feature, and were independently lost during Rickettsiales diversification. In addition, preliminary analyses suggest that ATP/ADP translocase, the marker for energy parasitism, was acquired after the acquisition of type IV secretion systems during the emergence of the Rickettsiales.

Further exploration of the oceanic samples yielded the first draft genomes of Marine Group IV archaea, the closest known relatives of the Haloarchaea. The halophilic and generally aerobic Haloarchaea are thought to have evolved from an anaerobic methanogenic ancestor. The MG-IV genomes allowed us to study this enigmatic evolutionary transition. Preliminary ancestral reconstruction analyses suggest a gradual loss of methanogenesis and adaptation to an aerobic lifestyle, respectively.

The thesis further presents a new amplicon sequencing method that captures near full-length 16S and 23S rRNA genes of environmental prokaryotes. The method exploits PacBio's long read technology and the frequent proximity of these genes in prokaryotic genomes. Compared to traditional partial 16S amplicon sequencing, our method classifies environmental lineages that are distantly related to reference taxa more confidently.

In conclusion, this thesis provides new insights into the origins of mitochondria, Rickettsiales and Haloarchaea and illustrates the power of cultivation independent methods with respect to the study of microbial evolution.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. 71 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1539
Keyword
cultivation independent genomics, metagenomics, single-cell genomics, metagenomic binning, phylogenetics, phylogenomics, phylogenetic artefacts, comparative genomics, gene tree-species tree reconciliation, rRNA amplicon sequencing, Tara Oceans, origin of mitochondria, Alphaproteobacteria, Rickettsiales, Haloarchaea, endosymbiosis
National Category
Evolutionary Biology Evolutionary Biology
Research subject
Biology with specialization in Molecular Evolution
Identifiers
urn:nbn:se:uu:diva-327310 (URN)978-91-513-0025-2 (ISBN)
Public defence
2017-09-29, B/B22, Biomedical Center (BMC), Husargatan 3, Uppsala, 09:15 (English)
Opponent
Supervisors
Available from: 2017-09-08 Created: 2017-08-08 Last updated: 2017-10-17

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Martijn, JoranZaremba-Niedzwiedzka, KatarzynaViklund, JohanAndersson, Siv G EGuy, LionelEttema, Thijs J G

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Martijn, JoranZaremba-Niedzwiedzka, KatarzynaViklund, JohanAndersson, Siv G EGuy, LionelEttema, Thijs J G
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Molecular EvolutionScience for Life Laboratory, SciLifeLabDepartment of Medical Biochemistry and Microbiology
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