dr hab. Anna Karnkowska
Scientific interests
My research focuses on the diversity, evolution and ecology of eukaryotic microorganisms (Protista). I work on the evolution of the eukaryotic cell, including the topics of the origin, evolution and reduction of organelles of endosymbiotic origins, as well as horizontal gene transfer in Eukaryotes. I also study the diversity and the role of photosynthetic and parasitic eukaryotic microorganisms in water habitats.
Didactics
- Practical Bioinformatics
- Biology of eukaryotic microorganisms
- Evolutionism for Bioinformatics and systems biology
- Publication strategy
- Modern biology
Research projects
- Photosymbiosis in freshwater ciliates: elucidating its diversity, functioning and evolution with single-cell sequencing, Preludium BIS Grant, NCN
- Freshwater microbial communities in the eutrophication gradient: diversity and interactions of protists and bacteria (MicroDivEr), Opus Grant NCN
- Inverted light microscope for the single-cell isolation of microbial eukaryotes, EMBO Young Investigator Small Grant
- Establishing protocols for the long-read sequencing of microbial eukaryotes, EMBO Young Investigator Small Grant
- Evolution of phototrophy in eukaryotes, EMBO Installation Grant
- Evolution and function of the inverted repeats (IR) in plastid genomes of Euglenophyta, Sonata Grant NCN
Internships
- Roscoff Marine Station, Roscoff, Francja, September 2021
- Botany Department, University of British Columbia, Vancouver, Canada (scientific supervisor: Prof. Patrick Keeling), January 2016 – December 2016, Postdoc
- Department of Cell Biology, University of Alberta, Canada (scientific supervisor: Prof. Joel B. Dacks), April 2014 – September 2014, scientific internship
- Parasitology Department, Charles University in Prague, Czech Republic (scientific supervisor: Dr hab. Vladimir Hampl), January 2013 – December 2015, Postdoc.
Prizes and distinctions
- L’oreal-UNESCO for Women in Science Award (2021)
- Prof. Pieńkowski Award (2020)
- The Science and Higher Education Minister’s Stipend for outstanding young scientists (2018)
- Foundation for Polish Science Stipend START (2013)
- President of the Council of Ministers Award for PhD thesis (2012)
Selected publications
2022 |
Karlicki, Michał; Antonowicz, Stanisław; Karnkowska, Anna Tiara: deep learning-based classification system for eukaryotic sequences Journal Article Bioinformatics, 38 (2), pp. 344–350, 2022. @article{Karlicki_2021, title = {Tiara: deep learning-based classification system for eukaryotic sequences}, author = {Michał Karlicki and Stanisław Antonowicz and Anna Karnkowska}, editor = {Inanc Birol}, url = {https://doi.org/10.1093%2Fbioinformatics%2Fbtab672}, doi = {10.1093/bioinformatics/btab672}, year = {2022}, date = {2022-01-07}, journal = {Bioinformatics}, volume = {38}, number = {2}, pages = {344–350}, publisher = {Oxford University Press (OUP)}, abstract = {Abstract Motivation With a large number of metagenomic datasets becoming available, eukaryotic metagenomics emerged as a new challenge. The proper classification of eukaryotic nuclear and organellar genomes is an essential step toward a better understanding of eukaryotic diversity. Results We developed Tiara, a deep-learning-based approach for the identification of eukaryotic sequences in the metagenomic datasets. Its two-step classification process enables the classification of nuclear and organellar eukaryotic fractions and subsequently divides organellar sequences into plastidial and mitochondrial. Using the test dataset, we have shown that Tiara performed similarly to EukRep for prokaryotes classification and outperformed it for eukaryotes classification with lower calculation time. In the tests on the real data, Tiara performed better than EukRep in analyzing the small dataset representing eukaryotic cell microbiome and large dataset from the pelagic zone of oceans. Tiara is also the only available tool correctly classifying organellar sequences, which was confirmed by the recovery of nearly complete plastid and mitochondrial genomes from the test data and real metagenomic data. Availability and implementation Tiara is implemented in python 3.8, available at https://github.com/ibe-uw/tiara and tested on Unix-based systems. It is released under an open-source MIT license and documentation is available at https://ibe-uw.github.io/tiara. Version 1.0.1 of Tiara has been used for all benchmarks. Supplementary information Supplementary data are available at Bioinformatics online.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Abstract Motivation With a large number of metagenomic datasets becoming available, eukaryotic metagenomics emerged as a new challenge. The proper classification of eukaryotic nuclear and organellar genomes is an essential step toward a better understanding of eukaryotic diversity. Results We developed Tiara, a deep-learning-based approach for the identification of eukaryotic sequences in the metagenomic datasets. Its two-step classification process enables the classification of nuclear and organellar eukaryotic fractions and subsequently divides organellar sequences into plastidial and mitochondrial. Using the test dataset, we have shown that Tiara performed similarly to EukRep for prokaryotes classification and outperformed it for eukaryotes classification with lower calculation time. In the tests on the real data, Tiara performed better than EukRep in analyzing the small dataset representing eukaryotic cell microbiome and large dataset from the pelagic zone of oceans. Tiara is also the only available tool correctly classifying organellar sequences, which was confirmed by the recovery of nearly complete plastid and mitochondrial genomes from the test data and real metagenomic data. Availability and implementation Tiara is implemented in python 3.8, available at https://github.com/ibe-uw/tiara and tested on Unix-based systems. It is released under an open-source MIT license and documentation is available at https://ibe-uw.github.io/tiara. Version 1.0.1 of Tiara has been used for all benchmarks. Supplementary information Supplementary data are available at Bioinformatics online. |
Maciszewski, Kacper; Dabbagh, Nadja; Preisfeld, Angelika; Karnkowska, Anna Maturyoshka: A maturase inside a maturase, and other peculiarities of the novel chloroplast genomes of marine euglenophytes Journal Article Molecular Phylogenetics and Evolution, 170 , pp. 107441, 2022, ISSN: 1055-7903. @article{MACISZEWSKI2022107441, title = {Maturyoshka: A maturase inside a maturase, and other peculiarities of the novel chloroplast genomes of marine euglenophytes}, author = {Kacper Maciszewski and Nadja Dabbagh and Angelika Preisfeld and Anna Karnkowska}, url = {https://www.sciencedirect.com/science/article/pii/S1055790322000549}, doi = {https://doi.org/10.1016/j.ympev.2022.107441}, issn = {1055-7903}, year = {2022}, date = {2022-01-01}, journal = {Molecular Phylogenetics and Evolution}, volume = {170}, pages = {107441}, abstract = {Organellar genomes often carry group II introns, which occasionally encode proteins called maturases that are important for splicing. The number of introns varies substantially among various organellar genomes, and bursts of introns have been observed in multiple eukaryotic lineages, including euglenophytes, with more than 100 introns in their plastid genomes. To examine the evolutionary diversity and history of maturases, an essential gene family among euglenophytes, we searched for their homologs in newly sequenced and published plastid genomes representing all major euglenophyte lineages. We found that maturase content in plastid genomes has a patchy distribution, with a maximum of eight of them present in Eutreptiella eupharyngea. The most basal lineages of euglenophytes, Eutreptiales, share the highest number of maturases, but the lowest number of introns. We also identified a peculiar convoluted structure of a gene located in an intron, in a gene within an intron, within yet another gene, present in some Eutreptiales. Further investigation of functional domains of identified maturases show that most of them lost at least one of the functional domains, which implies that the patchy maturase distribution is due to frequent inactivation and eventual loss over time. Finally, we identified the diversified evolutionary origin of analysed maturases, which were acquired along with the green algal plastid or horizontally transferred. These findings indicate that euglenophytes' plastid maturases have experienced a surprisingly dynamic history due to gains from diversified donors, their retention, and loss.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Organellar genomes often carry group II introns, which occasionally encode proteins called maturases that are important for splicing. The number of introns varies substantially among various organellar genomes, and bursts of introns have been observed in multiple eukaryotic lineages, including euglenophytes, with more than 100 introns in their plastid genomes. To examine the evolutionary diversity and history of maturases, an essential gene family among euglenophytes, we searched for their homologs in newly sequenced and published plastid genomes representing all major euglenophyte lineages. We found that maturase content in plastid genomes has a patchy distribution, with a maximum of eight of them present in Eutreptiella eupharyngea. The most basal lineages of euglenophytes, Eutreptiales, share the highest number of maturases, but the lowest number of introns. We also identified a peculiar convoluted structure of a gene located in an intron, in a gene within an intron, within yet another gene, present in some Eutreptiales. Further investigation of functional domains of identified maturases show that most of them lost at least one of the functional domains, which implies that the patchy maturase distribution is due to frequent inactivation and eventual loss over time. Finally, we identified the diversified evolutionary origin of analysed maturases, which were acquired along with the green algal plastid or horizontally transferred. These findings indicate that euglenophytes' plastid maturases have experienced a surprisingly dynamic history due to gains from diversified donors, their retention, and loss. |
2021 |
Treitli, Sebastian Cristian; Peña-Diaz, Priscila; Hałakuc, Paweł; Karnkowska, Anna; Hampl, Vladimír High quality genome assembly of the amitochondriate eukaryote Monocercomonoides exilis Journal Article Microbial Genomics, 7 (12), pp. 000745, 2021, ISSN: 2057-5858. @article{mbs:/content/journal/mgen/10.1099/mgen.0.000745, title = {High quality genome assembly of the amitochondriate eukaryote Monocercomonoides exilis}, author = {Sebastian Cristian Treitli and Priscila Peña-Diaz and Paweł Hałakuc and Anna Karnkowska and Vladimír Hampl}, url = {https://www.microbiologyresearch.org/content/journal/mgen/10.1099/mgen.0.000745}, doi = {https://doi.org/10.1099/mgen.0.000745}, issn = {2057-5858}, year = {2021}, date = {2021-12-24}, journal = {Microbial Genomics}, volume = {7}, number = {12}, pages = {000745}, publisher = {Microbiology Society}, abstract = {Monocercomonoides exilis is considered the first known eukaryote to completely lack mitochondria. This conclusion is based primarily on a genomic and transcriptomic study which failed to identify any mitochondrial hallmark proteins. However, the available genome assembly has limited contiguity and around 1.5 % of the genome sequence is represented by unknown bases. To improve the contiguity, we re-sequenced the genome and transcriptome of M. exilis using Oxford Nanopore Technology (ONT). The resulting draft genome is assembled in 101 contigs with an N50 value of 1.38 Mbp, almost 20 times higher than the previously published assembly. Using a newly generated ONT transcriptome, we further improve the gene prediction and add high quality untranslated region (UTR) annotations, in which we identify two putative polyadenylation signals present in the 3′UTR regions and characterise the Kozak sequence in the 5′UTR regions. All these improvements are reflected by higher BUSCO genome completeness values. Regardless of an overall more complete genome assembly without missing bases and a better gene prediction, we still failed to identify any mitochondrial hallmark genes, thus further supporting the hypothesis on the absence of mitochondrion.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Monocercomonoides exilis is considered the first known eukaryote to completely lack mitochondria. This conclusion is based primarily on a genomic and transcriptomic study which failed to identify any mitochondrial hallmark proteins. However, the available genome assembly has limited contiguity and around 1.5 % of the genome sequence is represented by unknown bases. To improve the contiguity, we re-sequenced the genome and transcriptome of M. exilis using Oxford Nanopore Technology (ONT). The resulting draft genome is assembled in 101 contigs with an N50 value of 1.38 Mbp, almost 20 times higher than the previously published assembly. Using a newly generated ONT transcriptome, we further improve the gene prediction and add high quality untranslated region (UTR) annotations, in which we identify two putative polyadenylation signals present in the 3′UTR regions and characterise the Kozak sequence in the 5′UTR regions. All these improvements are reflected by higher BUSCO genome completeness values. Regardless of an overall more complete genome assembly without missing bases and a better gene prediction, we still failed to identify any mitochondrial hallmark genes, thus further supporting the hypothesis on the absence of mitochondrion. |
Kostygov, Alexei Y; Karnkowska, Anna; Votypka, Jan; Tashyreva, Daria; Maciszewski, Kacper; Yurchenko, Vyacheslav; Lukes, Julius Euglenozoa : taxonomy, diversity and ecology, symbioses and viruses Journal Article Open Biology, 11 (3), pp. 200407-200407, 2021, ISBN: 0000000337. @article{Kostygov2021, title = {Euglenozoa : taxonomy, diversity and ecology, symbioses and viruses}, author = {Alexei Y Kostygov and Anna Karnkowska and Jan Votypka and Daria Tashyreva and Kacper Maciszewski and Vyacheslav Yurchenko and Julius Lukes}, url = {https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.200407}, doi = {https://doi.org/10.1098/rsob.200407}, isbn = {0000000337}, year = {2021}, date = {2021-01-01}, journal = {Open Biology}, volume = {11}, number = {3}, pages = {200407-200407}, abstract = {Euglenozoa is a species-rich group of protists, which have extremely diverse lifestyles and a range of features that distinguish them from other eukaryotes. They are composed of free-living and parasitic kinetoplastids, mostly free-living diplonemids, heterotrophic and photosynthetic euglenids, as well as deep-sea symbiontids. Although they form a well-supported monophyletic group, these morphologically rather distinct groups are almost never treated together in a comparative manner, as attempted here. We present an updated taxonomy, complemented by photos of representative species, with notes on diversity, distribution and biology of euglenozoans. For kinetoplastids, we propose a significantly modified taxonomy that reflects the latest findings. Finally, we summarize what is known about viruses infecting euglenozoans, as well as their relationships with ecto- and endosymbiotic bacteria.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Euglenozoa is a species-rich group of protists, which have extremely diverse lifestyles and a range of features that distinguish them from other eukaryotes. They are composed of free-living and parasitic kinetoplastids, mostly free-living diplonemids, heterotrophic and photosynthetic euglenids, as well as deep-sea symbiontids. Although they form a well-supported monophyletic group, these morphologically rather distinct groups are almost never treated together in a comparative manner, as attempted here. We present an updated taxonomy, complemented by photos of representative species, with notes on diversity, distribution and biology of euglenozoans. For kinetoplastids, we propose a significantly modified taxonomy that reflects the latest findings. Finally, we summarize what is known about viruses infecting euglenozoans, as well as their relationships with ecto- and endosymbiotic bacteria. |
Karnkowska, Anna; Treitli, Sebastian Cristian; Pen, Priscila; Hałakuc, Paweł; Karnkowska, Anna; Hampl, Vladimir High quality genome assembly of the amitochondriate eukaryote Monocercomonoides exilis Journal Article Microbial Genomics, 2021. @article{Anna_Karnkowska_105272112, title = {High quality genome assembly of the amitochondriate eukaryote Monocercomonoides exilis}, author = {Anna Karnkowska and Sebastian Cristian Treitli and Priscila Pen and Paweł Hałakuc and Anna Karnkowska and Vladimir Hampl}, url = {http://doi.org/10.1099/mgen.0.000745}, doi = {10.1099/mgen.0.000745}, year = {2021}, date = {2021-01-01}, journal = {Microbial Genomics}, keywords = {}, pubstate = {published}, tppubtype = {article} } |
2020 |
Kayama, Motoki; Maciszewski, Kacper; Yabuki, Akinori; Miyashita, Hideaki; Karnkowska, Anna; Kamikawa, Ryoma Frontiers in Plant Science, 11 , pp. 1859 , 2020. @article{Kayama2020, title = {Highly reduced plastid genomes of the non-photosynthetic dictyochophyceans Pteridomonas spp. (Ochrophyta, SAR) are retained for tRNA-Glu-based organellar heme biosynthesis.}, author = {Motoki Kayama and Kacper Maciszewski and Akinori Yabuki and Hideaki Miyashita and Anna Karnkowska and Ryoma Kamikawa }, url = {https://www.frontiersin.org/articles/10.3389/fpls.2020.602455/full}, doi = {https://doi.org/10.3389/fpls.2020.602455}, year = {2020}, date = {2020-11-27}, journal = {Frontiers in Plant Science}, volume = {11}, pages = {1859 }, keywords = {}, pubstate = {published}, tppubtype = {article} } |
Lukešová, Soňa; Karlicki, Michał; Hadariová, Lucia Tomečková; Szabová, Jana; Karnkowska, Anna; Hampl, Vladimír Environmental Microbiology Reports, 12 (1), pp. 78-91, 2020. @article{https://doi.org/10.1111/1758-2229.12817, title = {Analyses of environmental sequences and two regions of chloroplast genomes revealed the presence of new clades of photosynthetic euglenids in marine environments}, author = {Soňa Lukešová and Michał Karlicki and Lucia Tomečková Hadariová and Jana Szabová and Anna Karnkowska and Vladimír Hampl}, url = {https://sfamjournals.onlinelibrary.wiley.com/doi/abs/10.1111/1758-2229.12817}, doi = {https://doi.org/10.1111/1758-2229.12817}, year = {2020}, date = {2020-01-01}, journal = {Environmental Microbiology Reports}, volume = {12}, number = {1}, pages = {78-91}, abstract = {Euglenophyceae are unicellular algae with the majority of their diversity known from small freshwater reservoirs. Only two dozen species have been described to occur in marine habitats, but their abundance and diversity remain unexplored. Phylogenetic studies revealed marine prasinophyte green alga, Pyramimonas parkeae, as the closest extant relative of the euglenophytes' plastid, but similarly to euglenophytes, our knowledge about the diversity of Pyramimonadales is limited. Here we explored Euglenophyceae and Pyramimonadales phylogenetic diversity in marine environmental samples. We yielded 18S rDNA and plastid 16S rDNA sequences deposited in public repositories and reconstructed Euglenophyceae reference trees. We searched high-throughput environmental sequences from the TARA Oceans expedition and Ocean Sampling Day initiative for 18S rDNA and 16S rDNA, placed them in the phylogenetic context and estimated their relative abundances. To avoid polymerase chain reaction (PCR) bias, we also exploited metagenomic data from the TARA Oceans expedition for the presence of rRNA sequences from these groups. Finally, we targeted these protists in coastal samples by specific PCR amplification of two parts of the plastid genome uniquely shared between euglenids and Pyramimonadales. All approaches revealed previously undetected, but relatively low-abundant lineages of marine Euglenophyceae. Surprisingly, some of those lineages are branching within the freshwater or brackish genera.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Euglenophyceae are unicellular algae with the majority of their diversity known from small freshwater reservoirs. Only two dozen species have been described to occur in marine habitats, but their abundance and diversity remain unexplored. Phylogenetic studies revealed marine prasinophyte green alga, Pyramimonas parkeae, as the closest extant relative of the euglenophytes' plastid, but similarly to euglenophytes, our knowledge about the diversity of Pyramimonadales is limited. Here we explored Euglenophyceae and Pyramimonadales phylogenetic diversity in marine environmental samples. We yielded 18S rDNA and plastid 16S rDNA sequences deposited in public repositories and reconstructed Euglenophyceae reference trees. We searched high-throughput environmental sequences from the TARA Oceans expedition and Ocean Sampling Day initiative for 18S rDNA and 16S rDNA, placed them in the phylogenetic context and estimated their relative abundances. To avoid polymerase chain reaction (PCR) bias, we also exploited metagenomic data from the TARA Oceans expedition for the presence of rRNA sequences from these groups. Finally, we targeted these protists in coastal samples by specific PCR amplification of two parts of the plastid genome uniquely shared between euglenids and Pyramimonadales. All approaches revealed previously undetected, but relatively low-abundant lineages of marine Euglenophyceae. Surprisingly, some of those lineages are branching within the freshwater or brackish genera. |
2019 |
Maciszewski, Kacper; Karnkowska, Anna Should I stay or should I go? Retention and loss of components in vestigial endosymbiotic organelles Journal Article Current Opinion in Genetics & Development, 58-59 , pp. 33-39, 2019, ISSN: 0959-437X, (Evolutionary genetics). @article{MACISZEWSKI201933, title = {Should I stay or should I go? Retention and loss of components in vestigial endosymbiotic organelles}, author = {Kacper Maciszewski and Anna Karnkowska}, url = {https://www.sciencedirect.com/science/article/pii/S0959437X19300425}, doi = {https://doi.org/10.1016/j.gde.2019.07.013}, issn = {0959-437X}, year = {2019}, date = {2019-01-01}, journal = {Current Opinion in Genetics & Development}, volume = {58-59}, pages = {33-39}, abstract = {Our knowledge on the variability of the reduced forms of endosymbiotic organelles – mitochondria and plastids – is expanding rapidly, thanks to growing interest in peculiar microbial eukaryotes, along with the availability of the methods used in modern genomics and transcriptomics. The aim of this work is to highlight the most recent advances in understanding these organelles’ diversity, physiology and evolution. We also outline the known mechanisms behind the convergence of traits between organelles which have undergone reduction independently, the importance of the earliest evolutionary events in determining the vestigial organelles’ eventual fate, and a proposed classification of nonphotosynthetic plastids.}, note = {Evolutionary genetics}, keywords = {}, pubstate = {published}, tppubtype = {article} } Our knowledge on the variability of the reduced forms of endosymbiotic organelles – mitochondria and plastids – is expanding rapidly, thanks to growing interest in peculiar microbial eukaryotes, along with the availability of the methods used in modern genomics and transcriptomics. The aim of this work is to highlight the most recent advances in understanding these organelles’ diversity, physiology and evolution. We also outline the known mechanisms behind the convergence of traits between organelles which have undergone reduction independently, the importance of the earliest evolutionary events in determining the vestigial organelles’ eventual fate, and a proposed classification of nonphotosynthetic plastids. |
Han, Kwi Young; Maciszewski, Kacper; Graf, Louis; Yang, Ji Hyun; Andersen, Robert A; Karnkowska, Anna; Yoon, Hwan Su Dictyochophyceae Plastid Genomes Reveal Unusual Variability in Their Organization Journal Article Journal of Phycology, 55 (5), pp. 1166-1180, 2019. @article{https://doi.org/10.1111/jpy.12904, title = {Dictyochophyceae Plastid Genomes Reveal Unusual Variability in Their Organization}, author = {Kwi Young Han and Kacper Maciszewski and Louis Graf and Ji Hyun Yang and Robert A Andersen and Anna Karnkowska and Hwan Su Yoon}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/jpy.12904}, doi = {https://doi.org/10.1111/jpy.12904}, year = {2019}, date = {2019-01-01}, journal = {Journal of Phycology}, volume = {55}, number = {5}, pages = {1166-1180}, abstract = {Dictyochophyceae (silicoflagellates) are unicellular freshwater and marine algae (Heterokontophyta, stramenopiles). Despite their abundance in global oceans and potential ecological significance, discovered in recent years, neither nuclear nor organellar genomes of representatives of this group were sequenced until now. Here, we present the first complete plastid genome sequences of Dictyochophyceae, obtained from four species: Dictyocha speculum, Rhizochromulina marina, Florenciella parvula and Pseudopedinella elastica. Despite their comparable size and genetic content, these four plastid genomes exhibit variability in their organization: plastid genomes of F. parvula and P. elastica possess conventional quadripartite structure with a pair of inverted repeats, R. marina instead possesses two direct repeats with the same orientation and D. speculum possesses no repeats at all. We also observed a number of unusual traits in the plastid genome of D. speculum, including expansion of the intergenic regions, presence of an intron in the otherwise non-intron-bearing psaA gene, and an additional copy of the large subunit of RuBisCO gene (rbcL), the last of which has never been observed in any plastid genome. We conclude that despite noticeable gene content similarities between the plastid genomes of Dictyochophyceae and their relatives (pelagophytes, diatoms), the number of distinctive features observed in this lineage strongly suggests that additional taxa require further investigation.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Dictyochophyceae (silicoflagellates) are unicellular freshwater and marine algae (Heterokontophyta, stramenopiles). Despite their abundance in global oceans and potential ecological significance, discovered in recent years, neither nuclear nor organellar genomes of representatives of this group were sequenced until now. Here, we present the first complete plastid genome sequences of Dictyochophyceae, obtained from four species: Dictyocha speculum, Rhizochromulina marina, Florenciella parvula and Pseudopedinella elastica. Despite their comparable size and genetic content, these four plastid genomes exhibit variability in their organization: plastid genomes of F. parvula and P. elastica possess conventional quadripartite structure with a pair of inverted repeats, R. marina instead possesses two direct repeats with the same orientation and D. speculum possesses no repeats at all. We also observed a number of unusual traits in the plastid genome of D. speculum, including expansion of the intergenic regions, presence of an intron in the otherwise non-intron-bearing psaA gene, and an additional copy of the large subunit of RuBisCO gene (rbcL), the last of which has never been observed in any plastid genome. We conclude that despite noticeable gene content similarities between the plastid genomes of Dictyochophyceae and their relatives (pelagophytes, diatoms), the number of distinctive features observed in this lineage strongly suggests that additional taxa require further investigation. |
Karnkowska, Anna; Treitli, Sebastian C; Brzoň, Ondřej; Novák, Lukáš; Vacek, Vojtěch; Soukal, Petr; Barlow, Lael D; Herman, Emily K; Pipaliya, Shweta V; Pánek, Tomáš; Žihala, David; Petrželková, Romana; Butenko, Anzhelika; Eme, Laura; Stairs, Courtney W; Roger, Andrew J; Eliáš, Marek; Dacks, Joel B; Hampl, Vladimír The Oxymonad Genome Displays Canonical Eukaryotic Complexity in the Absence of a Mitochondrion Journal Article Molecular Biology and Evolution, 36 (10), pp. 2292-2312, 2019, ISSN: 0737-4038. @article{10.1093/molbev/msz147, title = {The Oxymonad Genome Displays Canonical Eukaryotic Complexity in the Absence of a Mitochondrion}, author = {Anna Karnkowska and Sebastian C Treitli and Ondřej Brzoň and Lukáš Novák and Vojtěch Vacek and Petr Soukal and Lael D Barlow and Emily K Herman and Shweta V Pipaliya and Tomáš Pánek and David Žihala and Romana Petrželková and Anzhelika Butenko and Laura Eme and Courtney W Stairs and Andrew J Roger and Marek Eliáš and Joel B Dacks and Vladimír Hampl}, url = {https://doi.org/10.1093/molbev/msz147}, doi = {10.1093/molbev/msz147}, issn = {0737-4038}, year = {2019}, date = {2019-01-01}, journal = {Molecular Biology and Evolution}, volume = {36}, number = {10}, pages = {2292-2312}, abstract = {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.}, keywords = {}, pubstate = {published}, tppubtype = {article} } 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. |
2018 |
Karnkowska, Anna; Bennett, Matthew S; Triemer, Richard E Dynamic evolution of inverted repeats in Euglenophyta plastid genomes Journal Article Scientific Reports, 8 (1), pp. 16071, 2018, ISSN: 2045-2322. @article{Karnkowska2018, title = {Dynamic evolution of inverted repeats in Euglenophyta plastid genomes}, author = {Anna Karnkowska and Matthew S Bennett and Richard E Triemer}, url = {https://doi.org/10.1038/s41598-018-34457-w}, doi = {10.1038/s41598-018-34457-w}, issn = {2045-2322}, year = {2018}, date = {2018-01-01}, journal = {Scientific Reports}, volume = {8}, number = {1}, pages = {16071}, abstract = {Photosynthetic euglenids (Euglenophyta) are a monophyletic group of unicellular eukaryotes characterized by the presence of plastids, which arose as the result of the secondary endosymbiosis. Many Euglenophyta plastid (pt) genomes have been characterized recently, but they represented mainly one family – Euglenaceae. Here, we report a comparative analysis of plastid genomes from eight representatives of the family Phacaceae. Newly sequenced plastid genomes share a number of features including synteny and gene content, except for genes mat2 and mat5 encoding maturases. The observed diversity of intron number and presence/absence of maturases corroborated previously suggested correlation between the number of maturases in the pt genome and intron proliferation. Surprisingly, pt genomes of taxa belonging to Discoplastis and Lepocinclis encode two inverted repeat (IR) regions containing the rDNA operon, which are absent from the Euglenaceae. By mapping the presence/absence of IR region on the obtained phylogenomic tree, we reconstructed the most probable events in the evolution of IRs in the Euglenophyta. Our study highlights the dynamic nature of the Euglenophyta plastid genome, in particular with regards to the IR regions that underwent losses repeatedly.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Photosynthetic euglenids (Euglenophyta) are a monophyletic group of unicellular eukaryotes characterized by the presence of plastids, which arose as the result of the secondary endosymbiosis. Many Euglenophyta plastid (pt) genomes have been characterized recently, but they represented mainly one family – Euglenaceae. Here, we report a comparative analysis of plastid genomes from eight representatives of the family Phacaceae. Newly sequenced plastid genomes share a number of features including synteny and gene content, except for genes mat2 and mat5 encoding maturases. The observed diversity of intron number and presence/absence of maturases corroborated previously suggested correlation between the number of maturases in the pt genome and intron proliferation. Surprisingly, pt genomes of taxa belonging to Discoplastis and Lepocinclis encode two inverted repeat (IR) regions containing the rDNA operon, which are absent from the Euglenaceae. By mapping the presence/absence of IR region on the obtained phylogenomic tree, we reconstructed the most probable events in the evolution of IRs in the Euglenophyta. Our study highlights the dynamic nature of the Euglenophyta plastid genome, in particular with regards to the IR regions that underwent losses repeatedly. |
Strassert, Jürgen F H; Karnkowska, Anna; Hehenberger, Elisabeth; del Campo, Javier; Kolisko, Martin; Okamoto, Noriko; Burki, Fabien; Janouškovec, Jan; Poirier, Camille; Leonard, Guy; Hallam, Steven J; Richards, Thomas A; Worden, Alexandra Z; Santoro, Alyson E; Keeling, Patrick J Single cell genomics of uncultured marine alveolates shows paraphyly of basal dinoflagellates Journal Article The ISME Journal, 12 (1), pp. 304–308, 2018, ISSN: 1751-7370. @article{Strassert2018, title = {Single cell genomics of uncultured marine alveolates shows paraphyly of basal dinoflagellates}, author = {Jürgen F H Strassert and Anna Karnkowska and Elisabeth Hehenberger and Javier del Campo and Martin Kolisko and Noriko Okamoto and Fabien Burki and Jan Janouškovec and Camille Poirier and Guy Leonard and Steven J Hallam and Thomas A Richards and Alexandra Z Worden and Alyson E Santoro and Patrick J Keeling}, url = {https://doi.org/10.1038/ismej.2017.167}, doi = {10.1038/ismej.2017.167}, issn = {1751-7370}, year = {2018}, date = {2018-01-01}, journal = {The ISME Journal}, volume = {12}, number = {1}, pages = {304--308}, abstract = {Marine alveolates (MALVs) are diverse and widespread early-branching dinoflagellates, but most knowledge of the group comes from a few cultured species that are generally not abundant in natural samples, or from diversity analyses of PCR-based environmental SSU rRNA gene sequences. To more broadly examine MALV genomes, we generated single cell genome sequences from seven individually isolated cells. Genes expected of heterotrophic eukaryotes were found, with interesting exceptions like presence of proteorhodopsin and vacuolar H+-pyrophosphatase. Phylogenetic analysis of concatenated SSU and LSU rRNA gene sequences provided strong support for the paraphyly of MALV lineages. Dinoflagellate viral nucleoproteins were found only in MALV groups that branched as sister to dinokaryotes. Our findings indicate that multiple independent origins of several characteristics early in dinoflagellate evolution, such as a parasitic life style, underlie the environmental diversity of MALVs, and suggest they have more varied trophic modes than previously thought.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Marine alveolates (MALVs) are diverse and widespread early-branching dinoflagellates, but most knowledge of the group comes from a few cultured species that are generally not abundant in natural samples, or from diversity analyses of PCR-based environmental SSU rRNA gene sequences. To more broadly examine MALV genomes, we generated single cell genome sequences from seven individually isolated cells. Genes expected of heterotrophic eukaryotes were found, with interesting exceptions like presence of proteorhodopsin and vacuolar H+-pyrophosphatase. Phylogenetic analysis of concatenated SSU and LSU rRNA gene sequences provided strong support for the paraphyly of MALV lineages. Dinoflagellate viral nucleoproteins were found only in MALV groups that branched as sister to dinokaryotes. Our findings indicate that multiple independent origins of several characteristics early in dinoflagellate evolution, such as a parasitic life style, underlie the environmental diversity of MALVs, and suggest they have more varied trophic modes than previously thought. |
2016 |
Karnkowska, Anna; Hampl, Vladimir The curious case of vanishing mitochondria Journal Article Microbial Cell, 3 (10), pp. 491–494, 2016, ISSN: 23112638. @article{Karnkowska2016, title = {The curious case of vanishing mitochondria}, author = {Anna Karnkowska and Vladimir Hampl}, url = {http://microbialcell.com/researcharticles/the-curious-case-of-vanishing-mitochondria/}, doi = {10.15698/mic2016.10.531}, issn = {23112638}, year = {2016}, date = {2016-10-01}, journal = {Microbial Cell}, volume = {3}, number = {10}, pages = {491--494}, abstract = {Due to their involvement in the energy metabolism, mitochondria are essential for most eukaryotic cells. Microbial eukaryotes living in low oxygen environments possess reduced forms of mitochondria, namely mitochondrion-related organelles (MROs). These do not produce ATP by oxidative phosphorylation on their membranes and some do not produce ATP at all. Still, they are indispensable because of other essential functions such as iron-sulphur (Fe-S) cluster assembly. Recently, the first microbial eukaryote with neither mitochondrion nor MRO was characterized – Monocercomonoides sp. Genome and transcriptome sequencing of Monocercomonoides revealed that it lacks all hallmark mitochondrial proteins. Crucially, the essential mitochondrial pathway for the Fe-S cluster assembly (ISC) was replaced by a bacterial sulphur mobilization (SUF) system. The discovery of such bona fide amitochondriate eukaryote broadens our knowledge about the diversity and plasticity of eukaryotic cells and provides a substantial contribution to our understanding of eukaryotic cell evolution.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Due to their involvement in the energy metabolism, mitochondria are essential for most eukaryotic cells. Microbial eukaryotes living in low oxygen environments possess reduced forms of mitochondria, namely mitochondrion-related organelles (MROs). These do not produce ATP by oxidative phosphorylation on their membranes and some do not produce ATP at all. Still, they are indispensable because of other essential functions such as iron-sulphur (Fe-S) cluster assembly. Recently, the first microbial eukaryote with neither mitochondrion nor MRO was characterized – Monocercomonoides sp. Genome and transcriptome sequencing of Monocercomonoides revealed that it lacks all hallmark mitochondrial proteins. Crucially, the essential mitochondrial pathway for the Fe-S cluster assembly (ISC) was replaced by a bacterial sulphur mobilization (SUF) system. The discovery of such bona fide amitochondriate eukaryote broadens our knowledge about the diversity and plasticity of eukaryotic cells and provides a substantial contribution to our understanding of eukaryotic cell evolution. |
Karnkowska, Anna; Vacek, Vojtěch; Zubáčová, Zuzana; Treitli, Sebastian C; Petrželková, Romana; Eme, Laura; Novák, Lukáš; Žárský, Vojtěch; Barlow, Lael D; Herman, Emily K; Soukal, Petr; Hroudová, Miluše; Doležal, Pavel; Stairs, Courtney W; Roger, Andrew J; Eliáš, Marek; Dacks, Joel B; Vlček, Čestmír; Hampl, Vladimír A Eukaryote without a Mitochondrial Organelle Journal Article Current Biology, 26 (10), pp. 1274-1284, 2016, ISSN: 0960-9822. @article{KARNKOWSKA20161274, title = {A Eukaryote without a Mitochondrial Organelle}, author = {Anna Karnkowska and Vojtěch Vacek and Zuzana Zubáčová and Sebastian C Treitli and Romana Petrželková and Laura Eme and Lukáš Novák and Vojtěch Žárský and Lael D Barlow and Emily K Herman and Petr Soukal and Miluše Hroudová and Pavel Doležal and Courtney W Stairs and Andrew J Roger and Marek Eliáš and Joel B Dacks and Čestmír Vlček and Vladimír Hampl}, url = {https://www.sciencedirect.com/science/article/pii/S0960982216302639}, doi = {https://doi.org/10.1016/j.cub.2016.03.053}, issn = {0960-9822}, year = {2016}, date = {2016-01-01}, journal = {Current Biology}, volume = {26}, number = {10}, pages = {1274-1284}, abstract = {Summary The presence of mitochondria and related organelles in every studied eukaryote supports the view that mitochondria are essential cellular components. Here, we report the genome sequence of a microbial eukaryote, the oxymonad Monocercomonoides sp., which revealed that this organism lacks all hallmark mitochondrial proteins. Crucially, the mitochondrial iron-sulfur cluster assembly pathway, thought to be conserved in virtually all eukaryotic cells, has been replaced by a cytosolic sulfur mobilization system (SUF) acquired by lateral gene transfer from bacteria. In the context of eukaryotic phylogeny, our data suggest that Monocercomonoides is not primitively amitochondrial but has lost the mitochondrion secondarily. This is the first example of a eukaryote lacking any form of a mitochondrion, demonstrating that this organelle is not absolutely essential for the viability of a eukaryotic cell.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Summary The presence of mitochondria and related organelles in every studied eukaryote supports the view that mitochondria are essential cellular components. Here, we report the genome sequence of a microbial eukaryote, the oxymonad Monocercomonoides sp., which revealed that this organism lacks all hallmark mitochondrial proteins. Crucially, the mitochondrial iron-sulfur cluster assembly pathway, thought to be conserved in virtually all eukaryotic cells, has been replaced by a cytosolic sulfur mobilization system (SUF) acquired by lateral gene transfer from bacteria. In the context of eukaryotic phylogeny, our data suggest that Monocercomonoides is not primitively amitochondrial but has lost the mitochondrion secondarily. This is the first example of a eukaryote lacking any form of a mitochondrion, demonstrating that this organelle is not absolutely essential for the viability of a eukaryotic cell. |
2015 |
Karnkowska, Anna; Bennett, Matthew S; Watza, Donovan; Kim, Jong Im; Zakryś, Bożena; Triemer, Richard E Journal of Eukaryotic Microbiology, 62 (3), pp. 362-373, 2015. @article{https://doi.org/10.1111/jeu.12192, title = {Phylogenetic Relationships and Morphological Character Evolution of Photosynthetic Euglenids (Excavata) Inferred from Taxon-rich Analyses of Five Genes}, author = {Anna Karnkowska and Matthew S Bennett and Donovan Watza and Jong Im Kim and Bożena Zakryś and Richard E Triemer}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/jeu.12192}, doi = {https://doi.org/10.1111/jeu.12192}, year = {2015}, date = {2015-01-01}, journal = {Journal of Eukaryotic Microbiology}, volume = {62}, number = {3}, pages = {362-373}, abstract = {Abstract Photosynthetic euglenids acquired chloroplasts by secondary endosymbiosis, which resulted in changes to their mode of nutrition and affected the evolution of their morphological characters. Mapping morphological characters onto a reliable molecular tree could elucidate major trends of those changes. We analyzed nucleotide sequence data from regions of three nuclear-encoded genes (nSSU, nLSU, hsp90), one chloroplast-encoded gene (cpSSU) and one nuclear-encoded chloroplast gene (psbO) to estimate phylogenetic relationships among 59 photosynthetic euglenid species. Our results were consistent with previous works; most genera were monophyletic, except for the polyphyletic genus Euglena, and the paraphyletic genus Phacus. We also analyzed character evolution in photosynthetic euglenids using our phylogenetic tree and eight morphological traits commonly used for generic and species diagnoses, including: characters corresponding to well-defined clades, apomorphies like presence of lorica and mucilaginous stalks, and homoplastic characters like rigid cells and presence of large paramylon grains. This research indicated that pyrenoids were lost twice during the evolution of phototrophic euglenids, and that mucocysts, which only occur in the genus Euglena, evolved independently at least twice. In contrast, the evolution of cell shape and chloroplast morphology was difficult to elucidate, and could not be unambiguously reconstructed in our analyses.}, keywords = {}, pubstate = {published}, tppubtype = {article} } Abstract Photosynthetic euglenids acquired chloroplasts by secondary endosymbiosis, which resulted in changes to their mode of nutrition and affected the evolution of their morphological characters. Mapping morphological characters onto a reliable molecular tree could elucidate major trends of those changes. We analyzed nucleotide sequence data from regions of three nuclear-encoded genes (nSSU, nLSU, hsp90), one chloroplast-encoded gene (cpSSU) and one nuclear-encoded chloroplast gene (psbO) to estimate phylogenetic relationships among 59 photosynthetic euglenid species. Our results were consistent with previous works; most genera were monophyletic, except for the polyphyletic genus Euglena, and the paraphyletic genus Phacus. We also analyzed character evolution in photosynthetic euglenids using our phylogenetic tree and eight morphological traits commonly used for generic and species diagnoses, including: characters corresponding to well-defined clades, apomorphies like presence of lorica and mucilaginous stalks, and homoplastic characters like rigid cells and presence of large paramylon grains. This research indicated that pyrenoids were lost twice during the evolution of phototrophic euglenids, and that mucocysts, which only occur in the genus Euglena, evolved independently at least twice. In contrast, the evolution of cell shape and chloroplast morphology was difficult to elucidate, and could not be unambiguously reconstructed in our analyses. |