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Publications (10 of 13) Show all publications
Hess, S., Eme, L., Roger, A. J. & Simpson, A. G. B. (2019). A natural toroidal microswimmer with a rotary eukaryotic flagellum. Nature Microbiology, 4(10), 1620-1626
Open this publication in new window or tab >>A natural toroidal microswimmer with a rotary eukaryotic flagellum
2019 (English)In: Nature Microbiology, E-ISSN 2058-5276, Vol. 4, no 10, p. 1620-1626Article in journal (Refereed) Published
Abstract [en]

We describe Idionectes vortex gen. nov., sp. nov., a unicellular microeukaryote that swims by continuous inversion of its surface, similar to a vortex ring. This previously unreported mode of motility approximates a hypothetical concept called the 'toroidal swimmer', in which a doughnut-shaped object rotates around its circular axis and travels in the opposite direction to its outer surface motion. During swimming, the flagellum of Idionectes rotates relative to its cell body, which is normally a hallmark of prokaryotic rather than eukaryotic flagella.

National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-395785 (URN)10.1038/s41564-019-0478-6 (DOI)000487286800007 ()31182800 (PubMedID)
Funder
German Research Foundation (DFG), HE 7560/1-1
Available from: 2019-10-28 Created: 2019-10-28 Last updated: 2019-10-28Bibliographically approved
Seitz, K. W., Dombrowski, N., Eme, L., Spang, A., Lombard, J., Sieber, J. R., . . . Baker, B. J. (2019). Asgard archaea capable of anaerobic hydrocarbon cycling. Nature Communications, 10, Article ID 1822.
Open this publication in new window or tab >>Asgard archaea capable of anaerobic hydrocarbon cycling
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2019 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 10, article id 1822Article in journal (Refereed) Published
Abstract [en]

Large reservoirs of natural gas in the oceanic subsurface sustain complex communities of anaerobic microbes, including archaeal lineages with potential to mediate oxidation of hydrocarbons such as methane and butane. Here we describe a previously unknown archaeal phylum, Helarchaeota, belonging to the Asgard superphylum and with the potential for hydrocarbon oxidation. We reconstruct Helarchaeota genomes from metagenomic data derived from hydrothermal deep-sea sediments in the hydrocarbon-rich Guaymas Basin. The genomes encode methyl-CoM reductase-like enzymes that are similar to those found in butane-oxidizing archaea, as well as several enzymes potentially involved in alkyl-CoA oxidation and the Wood-Ljungdahl pathway. We suggest that members of the Helarchaeota have the potential to activate and subsequently anaerobically oxidize hydrothermally generated short-chain hydrocarbons.

Place, publisher, year, edition, pages
NATURE PUBLISHING GROUP, 2019
National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-383164 (URN)10.1038/s41467-019-09364-x (DOI)000465200000003 ()31015394 (PubMedID)
Funder
Swedish Research Council, 2016-03559EU, European Research Council, 310039-PUZZLE_CELLSwedish Foundation for Strategic Research , SSF-FFL5Swedish Research Council, 2015-04959EU, Horizon 2020, 704263
Available from: 2019-05-10 Created: 2019-05-10 Last updated: 2019-05-10Bibliographically approved
Spang, A., Stairs, C. W., Dombrowski, N., Eme, L., Lombard, J., Caceres, E. F., . . . Ettema, T. J. G. (2019). Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism. Nature Microbiology, 4(7), 1138-1148
Open this publication in new window or tab >>Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism
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2019 (English)In: Nature Microbiology, E-ISSN 2058-5276, Vol. 4, no 7, p. 1138-1148Article in journal (Refereed) Published
Abstract [en]

The origin of eukaryotes represents an unresolved puzzle in evolutionary biology. Current research suggests that eukaryotes evolved from a merger between a host of archaeal descent and an alphaproteobacterial endosymbiont. The discovery of the Asgard archaea, a proposed archaeal superphylum that includes Lokiarchaeota, Thorarchaeota, Odinarchaeota and Heimdallarchaeota suggested to comprise the closest archaeal relatives of eukaryotes, has helped to elucidate the identity of the putative archaeal host. Whereas Lokiarchaeota are assumed to employ a hydrogen-dependent metabolism, little is known about the metabolic potential of other members of the Asgard superphylum. We infer the central metabolic pathways of Asgard archaea using comparative genomics and phylogenetics to be able to refine current models for the origin of eukaryotes. Our analyses indicate that Thorarchaeota and Lokiarchaeota encode proteins necessary for carbon fixation via the Wood-Ljungdahl pathway and for obtaining reducing equivalents from organic substrates. By contrast, Heimdallarchaeum LC2 and LC3 genomes encode enzymes potentially enabling the oxidation of organic substrates using nitrate or oxygen as electron acceptors. The gene repertoire of Heimdallarchaeum AB125 and Odinarchaeum indicates that these organisms can ferment organic substrates and conserve energy by coupling ferredoxin reoxidation to respiratory proton reduction. Altogether, our genome analyses suggest that Asgard representatives are primarily organoheterotrophs with variable capacity for hydrogen consumption and production. On this basis, we propose the 'reverse flow model', an updated symbiogenetic model for the origin of eukaryotes that involves electron or hydrogen flow from an organoheterotrophic archaeal host to a bacterial symbiont.

Place, publisher, year, edition, pages
NATURE PUBLISHING GROUP, 2019
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-393531 (URN)10.1038/s41564-019-0406-9 (DOI)000480348200010 ()30936488 (PubMedID)
Funder
EU, European Research Council, 310039-PUZZLE_CELLSwedish Foundation for Strategic Research , SSF-FFL5Swedish Research Council, 2015-04959Swedish Research Council, 2016-03559Australian Research Council, DE170100310Australian Research Council, DP180101762
Available from: 2019-09-24 Created: 2019-09-24 Last updated: 2019-09-24Bibliographically approved
Karnkowska, A., Treitli, S. C., Brzon, O., Novak, L., Vacek, V., Soukal, P., . . . Hampl, V. (2019). The Oxymonad Genome Displays Canonical Eukaryotic Complexity in the Absence of a Mitochondrion. Molecular biology and evolution, 36(10), 2292-2312
Open this publication in new window or tab >>The Oxymonad Genome Displays Canonical Eukaryotic Complexity in the Absence of a Mitochondrion
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2019 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 36, no 10, p. 2292-2312Article in journal (Refereed) Published
Abstract [en]

The discovery that the protist Monocercomonoides exilis completely lacks mitochondria demonstrates that these organelles are not absolutely essential to eukaryotic cells. However, the degree to which the metabolism and cellular systems of this organism have adapted to the loss of mitochondria is unknown. Here, we report an extensive analysis of the M. exilis genome to address this question. Unexpectedly, we find that M. exilis genome structure and content is similar in complexity to other eukaryotes and less "reduced" than genomes of some other protists from the Metamonada group to which it belongs. Furthermore, the predicted cytoskeletal systems, the organization of endomembrane systems, and biosynthetic pathways also display canonical eukaryotic complexity. The only apparent preadaptation that permitted the loss of mitochondria was the acquisition of the SUF system for Fe-S cluster assembly and the loss of glycine cleavage system. Changes in other systems, including in amino acid metabolism and oxidative stress response, were coincident with the loss of mitochondria but are likely adaptations to the microaerophilic and endobiotic niche rather than the mitochondrial loss per se. Apart from the lack of mitochondria and peroxisomes, we show that M. exilis is a fully elaborated eukaryotic cell that is a promising model system in which eukaryotic cell biology can be investigated in the absence of mitochondria.

Place, publisher, year, edition, pages
OXFORD UNIV PRESS, 2019
Keywords
amitochondrial eukaryote, cell biology, Monocercomonoides, oxymonads, protist genomics
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:uu:diva-400822 (URN)10.1093/molbev/msz147 (DOI)000501734200017 ()31387118 (PubMedID)
Funder
EU, Horizon 2020, 771592
Available from: 2020-01-13 Created: 2020-01-13 Last updated: 2020-01-13Bibliographically approved
Spang, A., Eme, L., Saw, J. H., Fernández Cáceres, E., Zaremba-Niedzwiedzka, K., Lombard, J., . . . Ettema, T. J. G. (2018). Asgard archaea are the closest prokaryotic relatives of eukaryotes. PLoS Genetics, 14(3), Article ID e1007080.
Open this publication in new window or tab >>Asgard archaea are the closest prokaryotic relatives of eukaryotes
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2018 (English)In: PLoS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 14, no 3, article id e1007080Article in journal, Editorial material (Other academic) Published
National Category
Medical Genetics
Identifiers
urn:nbn:se:uu:diva-357040 (URN)10.1371/journal.pgen.1007080 (DOI)000428840600002 ()29596421 (PubMedID)
Funder
EU, European Research Council, 310039-PUZZLE_CELLSwedish Research Council, 2015-04959EU, Horizon 2020, 704263The Wenner-Gren Foundation, UPD2016-0072Swedish Foundation for Strategic Research , SSF-FFL5
Available from: 2018-08-10 Created: 2018-08-10 Last updated: 2018-10-23Bibliographically approved
Leger, M. M., Eme, L., Stairs, C. W. & Roger, A. J. (2018). Demystifying Eukaryote Lateral Gene Transfer. Bioessays, 40(5), Article ID 1700242.
Open this publication in new window or tab >>Demystifying Eukaryote Lateral Gene Transfer
2018 (English)In: Bioessays, ISSN 0265-9247, E-ISSN 1521-1878, Vol. 40, no 5, article id 1700242Article in journal (Refereed) Published
Abstract [en]

In a recent BioEssays paper [W. F. Martin, BioEssays 2017, 39, 1700115], William Martin sharply criticizes evolutionary interpretations that involve lateral gene transfer (LGT) into eukaryotic genomes. Most published examples of LGTs in eukaryotes, he suggests, are in fact contaminants, ancestral genes that have been lost from other extant lineages, or the result of artefactual phylogenetic inferences. Martin argues that, except for transfers that occurred from endosymbiotic organelles, eukaryote LGT is insignificant. Here, in reviewing this field, we seek to correct some of the misconceptions presented therein with regard to the evidence for LGT in eukaryotes.

Keywords
eukaryote genomes, horizontal gene transfer, lateral gene transfer
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-353361 (URN)10.1002/bies.201700242 (DOI)000430463500006 ()29543982 (PubMedID)
Funder
EU, European Research Council, ERC-2012-Co-616960]EU, Horizon 2020, 704263]
Available from: 2018-06-12 Created: 2018-06-12 Last updated: 2018-08-21Bibliographically approved
Lax, G., Eglit, Y., Eme, L., Bertrand, E. M., Roger, A. J. & Simpson, A. G. B. (2018). Hemimastigophora is a novel supra-kingdom-level lineage of eukaryotes [Letter to the editor]. Nature, 564(7736), 410-414
Open this publication in new window or tab >>Hemimastigophora is a novel supra-kingdom-level lineage of eukaryotes
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2018 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 564, no 7736, p. 410-414Article in journal, Letter (Refereed) Published
Abstract [en]

Almost all eukaryote life forms have now been placed within one of five to eight supra-kingdom-level groups using molecular phylogenetics(1-4). The 'phylum' Hemimastigophora is probably the most distinctive morphologically defined lineage that still awaits such a phylogenetic assignment. First observed in the nineteenth century, hemimastigotes are free-living predatory protists with two rows of flagella and a unique cell architecture(5-7); to our knowledge, no molecular sequence data or cultures are currently available for this group. Here we report phylogenomic analyses based on high-coverage, cultivation-independent transcriptomics that place Hemimastigophora outside of all established eukaryote supergroups. They instead comprise an independent supra-kingdom-level lineage that most likely forms a sister clade to the 'Diaphoretickes' half of eukaryote diversity (that is, the 'stramenopiles, alveolates and Rhizaria' supergroup (Sar), Archaeplastida and Cryptista, as well as other major groups). The previous ranking of Hemimastigophora as a phylum understates the evolutionary distinctiveness of this group, which has considerable importance for investigations into the deep-level evolutionary history of eukaryotic life-ranging from understanding the origins of fundamental cell systems to placing the root of the tree. We have also established the first culture of a hemimastigote (Hemimastix kukwesjijk sp. nov.), which will facilitate future genomic and cellbiological investigations into eukaryote evolution and the last eukaryotic common ancestor.

Place, publisher, year, edition, pages
NATURE PUBLISHING GROUP, 2018
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-372887 (URN)10.1038/s41586-018-0708-8 (DOI)000453834900060 ()30429611 (PubMedID)
Available from: 2019-01-09 Created: 2019-01-09 Last updated: 2019-01-09Bibliographically approved
Cenci, U., Sibbald, S. J., Curtis, B. A., Kamikawa, R., Eme, L., Moog, D., . . . Archibald, J. M. (2018). Nuclear genome sequence of the plastid-lacking cryptomonad Goniomonas avonlea provides insights into the evolution of secondary plastids. BMC Biology, 16, Article ID 137.
Open this publication in new window or tab >>Nuclear genome sequence of the plastid-lacking cryptomonad Goniomonas avonlea provides insights into the evolution of secondary plastids
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2018 (English)In: BMC Biology, ISSN 1741-7007, E-ISSN 1741-7007, Vol. 16, article id 137Article in journal (Refereed) Published
Abstract [en]

Background: The evolution of photosynthesis has been a major driver in eukaryotic diversification. Eukaryotes have acquired plastids (chloroplasts) either directly via the engulfment and integration of a photosynthetic cyanobacterium (primary endosymbiosis) or indirectly by engulfing a photosynthetic eukaryote (secondary or tertiary endosymbiosis). The timing and frequency of secondary endosymbiosis during eukaryotic evolution is currently unclear but may be resolved in part by studying cryptomonads, a group of single-celled eukaryotes comprised of both photosynthetic and non-photosynthetic species. While cryptomonads such as Guillardia theta harbor a red algal-derived plastid of secondary endosymbiotic origin, members of the sister group Goniomonadea lack plastids. Here, we present the genome of Goniomonas avonlea-the first for any goniomonad-to address whether Goniomonadea are ancestrally non-photosynthetic or whether they lost a plastid secondarily. Results: We sequenced the nuclear and mitochondrial genomes of Goniomonas avonlea and carried out a comparative analysis of Go. avonlea, Gu. theta, and other cryptomonads. The Go. avonlea genome assembly is similar to 92 Mbp in size, with 33,470 predicted protein-coding genes. Interestingly, some metabolic pathways (e.g., fatty acid biosynthesis) predicted to occur in the plastid and periplastidal compartment of Gu. theta appear to operate in the cytoplasm of Go. avonlea, suggesting that metabolic redundancies were generated during the course of secondary plastid integration. Other cytosolic pathways found in Go. avonlea are not found in Gu. theta, suggesting secondary loss in Gu. theta and other plastid-bearing cryptomonads. Phylogenetic analyses revealed no evidence for algal endosymbiont-derived genes in the Go. avonlea genome. Phylogenomic analyses point to a specific relationship between Cryptista (to which cryptomonads belong) and Archaeplastida. Conclusion: We found no convincing genomic or phylogenomic evidence that Go. avonlea evolved from a secondary red algal plastid-bearing ancestor, consistent with goniomonads being ancestrally non-photosynthetic eukaryotes. The Go. avonlea genome sheds light on the physiology of heterotrophic cryptomonads and serves as an important reference point for studying the metabolic "rewiring" that took place during secondary plastid integration in the ancestor of modern-day Cryptophyceae.

Keywords
Cryptomonads, Cryptophytes, Secondary endosymbiosis, Phylogenomics, Genome evolution
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-372444 (URN)10.1186/s12915-018-0593-5 (DOI)000451397800001 ()30482201 (PubMedID)
Available from: 2019-01-07 Created: 2019-01-07 Last updated: 2019-01-07Bibliographically approved
Raina, J.-B., Eme, L., Pollock, F. J., Spang, A., Archibald, J. M. & Williams, T. A. (2018). Symbiosis in the microbial world: from ecology to genome evolution. BIOLOGY OPEN, 7(2), Article ID UNSP bio032524.
Open this publication in new window or tab >>Symbiosis in the microbial world: from ecology to genome evolution
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2018 (English)In: BIOLOGY OPEN, ISSN 2046-6390, Vol. 7, no 2, article id UNSP bio032524Article, review/survey (Refereed) Published
Abstract [en]

The concept of symbiosis - defined in 1879 by de Bary as 'the living together of unlike organisms' - has a rich and convoluted history in biology. In part, because it questioned the concept of the individual, symbiosis fell largely outside mainstream science and has traditionally received less attention than other research disciplines. This is gradually changing. In nature organisms do not live in isolation but rather interact with, and are impacted by, diverse beings throughout their life histories. Symbiosis is now recognized as a central driver of evolution across the entire tree of life, including, for example, bacterial endosymbionts that provide insects with vital nutrients and the mitochondria that power our own cells. Symbioses between microbes and their multicellular hosts also underpin the ecological success of some of the most productive ecosystems on the planet, including hydrothermal vents and coral reefs. In November 2017, scientists working in fields spanning the life sciences came together at a Company of Biologists' workshop to discuss the origin, maintenance, and long-term implications of symbiosis from the complementary perspectives of cell biology, ecology, evolution and genomics, taking into account both model and non-model organisms. Here, we provide a brief synthesis of the fruitful discussions that transpired.

Keywords
Ecology, Evolution, Symbiosis
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-351598 (URN)10.1242/bio.032524 (DOI)000426390300001 ()29472284 (PubMedID)
Available from: 2018-05-29 Created: 2018-05-29 Last updated: 2018-08-21Bibliographically approved
Eme, L. & Ettema, T. J. G. (2018). The eukaryotic ancestor shapes up. Nature, 562(7727), 352-354
Open this publication in new window or tab >>The eukaryotic ancestor shapes up
2018 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 562, no 7727, p. 352-354Article in journal, Editorial material (Other academic) Published
Abstract [en]

Asgard archaea are the closest known relatives of nucleus-bearing organisms called eukaryotes. A study indicates that these archaea have a dynamic network of actin protein - a trait thought of as eukaryote-specific.

Place, publisher, year, edition, pages
Nature Publishing Group, 2018
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-369618 (URN)10.1038/d41586-018-06868-2 (DOI)000447807100047 ()
Available from: 2018-12-17 Created: 2018-12-17 Last updated: 2019-01-17Bibliographically approved
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ORCID iD: ORCID iD iconorcid.org/0000-0002-0510-8868

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