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Ken-ichiro Ishida - One of the best experts on this subject based on the ideXlab platform.
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Dinoflagellates with relic endosymbiont nuclei as models for elucidating organellogenesis
Proceedings of the National Academy of Sciences of the United States of America, 2020Co-Authors: Chihiro Sarai, Ken-ichiro Ishida, Goro Tanifuji, Takuro Nakayama, Ryoma Kamikawa, Kazuya Takahashi, Euki Yazaki, Eriko Matsuo, Hideaki Miyashita, Mitsunori IwatakiAbstract:Nucleomorphs are relic endosymbiont nuclei so far found only in two algal groups, cryptophytes and Chlorarachniophytes, which have been studied to model the evolutionary process of integrating an endosymbiont alga into a host-governed plastid (organellogenesis). However, past studies suggest that DNA transfer from the endosymbiont to host nuclei had already ceased in both cryptophytes and Chlorarachniophytes, implying that the organellogenesis at the genetic level has been completed in the two systems. Moreover, we have yet to pinpoint the closest free-living relative of the endosymbiotic alga engulfed by the ancestral Chlorarachniophyte or cryptophyte, making it difficult to infer how organellogenesis altered the endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which endosymbiont-to-host DNA transfer is on-going and for which endosymbiont/plastid origins can be inferred at a fine taxonomic scale. Here, we report two previously undescribed dinoflagellates, strains MGD and TGD, with green algal endosymbionts enclosing plastids as well as relic nuclei (nucleomorphs). We provide evidence for the presence of DNA in the two nucleomorphs and the transfer of endosymbiont genes to the host (dinoflagellate) genomes. Furthermore, DNA transfer between the host and endosymbiont nuclei was found to be in progress in both the MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the endosymbionts at the genus level. With the combined evidence, we conclude that the host–endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as models for elucidating organellogenesis.
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Dinoflagellates with relic endosymbiont nuclei as novel models for elucidating organellogenesis
bioRxiv, 2019Co-Authors: Chihiro Sarai, Ken-ichiro Ishida, Goro Tanifuji, Takuro Nakayama, Ryoma Kamikawa, Kazuya Takahashi, Hideaki Miyashita, Mitsunori Iwataki, Yuji InagakiAbstract:Nucleomorphs are relic endosymbiont nuclei so far found only in two algal groups, cryptophytes and Chlorarachniophytes, which have been studied to model the evolutionary process integrating an endosymbiont alga into be a host-governed plastid (organellogenesis). Nevertheless, past studies suggested that DNA transfer from the endosymbiont to host nuclei had already ceased in both cryptophytes and Chlorarachniophytes, implying that the organellogenesis at the genetic level has been completed in the two systems. Moreover, we have yet to pinpoint the closest free-living relative of the endosymbiotic alga engulfed by the ancestral Chlorarachniophyte or cryptophyte, making difficult to infer how organellogenesis altered the endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which from-endosymbiont-to-host DNA transfer is on-going and of which endosymbiont/plastid origins can be inferred at a fine taxonomic scale. Here, we report two previously undescribed dinoflagellates, strains MGD and TGD, with green algal endosymbionts enclosing plastids as well as relic nuclei (nucleomorphs). We provide the evidence for the presence of DNA in the two nucleomorphs and transfer of endosymbiont genes to the host (dinoflagellate) genomes. Furthermore, DNA transfer between the host and endosymbiont nuclei was found to be in progress in both MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the endosymbionts at the genus level. Combined, we conclude that the host-endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as new models for elucidating organellogenesis.
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Viridiuvalis adhaerens gen. et sp. nov., a novel colony-forming Chlorarachniophyte
Journal of Plant Research, 2017Co-Authors: Takashi Shiratori, Sakuya Fujita, Tenma Shimizu, Takeshi Nakayama, Ken-ichiro IshidaAbstract:A new Chlorarachniophyte, Viridiuvalis adhaerens gen. et sp. nov. was isolated from the mucus on a coral reef from Zanpa Beach, Okinawa, Japan. The main vegetative stage of V. adhaerens consisted of unicellular coccoid cells with cell walls, although sarcinoid colonies and uniflagellate zoospores were also observed. V. adhaerens had chloroplasts with nucleomorphs and pyrenoids that were completely embedded in the chloroplast. A deep plate-like invagination of the periplastidal compartment (PPC) almost partitioned the pyrenoid and chloroplast components, which were surrounded by two membranes. The nucleomorph was positioned in the base of the invagination of the PPC. Molecular phylogenetic analyses using rRNA genes showed that V. adhaerens branched as a sister lineage of the Amorphochlora clade. The sarcinoid colony, pyrenoid embedded in the chloroplast, and nucleomorph located at the base of the deep invagination of the PPC have not been reported in other Chlorarachniophytes. Based on these morphological and ultrastructural characteristics and the results of the molecular phylogenetic analyses, we propose V. adhaerens as a new genus and species of Chlorarachniophyte.
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diurnal transcriptional regulation of endosymbiotically derived genes in the Chlorarachniophyte bigelowiella natans
Genome Biology and Evolution, 2016Co-Authors: Shigekatsu Suzuki, Ken-ichiro Ishida, Yoshihisa HirakawaAbstract:Chlorarachniophyte algae possess complex plastids acquired by the secondary endosymbiosis of a green alga, and the plastids harbor a relict nucleus of the endosymbiont, the so-called nucleomorph. Due to massive gene transfer from the endosymbiont to the host, many proteins involved in plastid and nucleomorph are encoded by the nuclear genome. Genome sequences have provided a blueprint for the fate of endosymbiotically derived genes; however, transcriptional regulation of these genes remains poorly understood. To gain insight into the evolution of endosymbiotic genes, we performed genome-wide transcript profiling along the cell cycle of the Chlorarachniophyte Bigelowiella natans, synchronized by light and dark cycles. Our comparative analyses demonstrated that transcript levels of 7,751 nuclear genes (35.7% of 21,706 genes) significantly oscillated along the diurnal/cell cycles, and those included 780 and 147 genes for putative plastid and nucleomorph-targeted proteins, respectively. Clustering analysis of those genes revealed the existence of transcriptional networks related to specific biological processes such as photosynthesis, carbon metabolism, translation, and DNA replication. Interestingly, transcripts of many plastid-targeted proteins in B. natans were induced before dawn, unlike other photosynthetic organisms. In contrast to nuclear genes, 99% nucleomorph genes were found to be constitutively expressed during the cycles. We also found that the nucleomorph DNA replication would be controlled by a nucleus-encoded viral-like DNA polymerase. The results of this study suggest that nucleomorph genes have lost transcriptional regulation along the diurnal cycles, and nuclear genes exert control over the complex plastid including the nucleomorph.
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Plastid genome sequences of Gymnochlora stellata, Lotharella vacuolata, and Partenskyella glossopodia reveal remarkable structural conservation among Chlorarachniophyte species
Journal of Plant Research, 2016Co-Authors: Shigekatsu Suzuki, Yoshihisa Hirakawa, Rumiko Kofuji, Mamoru Sugita, Ken-ichiro IshidaAbstract:Chlorarachniophyte algae have complex plastids acquired by the uptake of a green algal endosymbiont, and this event is called secondary endosymbiosis. Interestingly, the plastids possess a relict endosymbiont nucleus, referred to as the nucleomorph, in the intermembrane space, and the nucleomorphs contain an extremely reduced and compacted genome in comparison with green algal nuclear genomes. Therefore, Chlorarachniophyte plastids consist of two endosymbiotically derived genomes, i.e., the plastid and nucleomorph genomes. To date, complete nucleomorph genomes have been sequenced in four different species, whereas plastid genomes have been reported in only two species in Chlorarachniophytes. To gain further insight into the evolution of endosymbiotic genomes in Chlorarachniophytes, we newly sequenced the plastid genomes of three species, Gymnochlora stellata , Lotharella vacuolata , and Partenskyella glossopodia . Our findings reveal that Chlorarachniophyte plastid genomes are highly conserved in size, gene content, and gene order among species, but their nucleomorph genomes are divergent in such features. Accordingly, the current architecture of the plastid genomes of Chlorarachniophytes evolved in a common ancestor, and changed very little during their subsequent diversification. Furthermore, our phylogenetic analyses using multiple plastid genes suggest that Chlorarachniophyte plastids are derived from a green algal lineage that is closely related to Bryopsidales in the Ulvophyceae group.
John M Archibald - One of the best experts on this subject based on the ideXlab platform.
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Nucleomorph genomes.
Annual review of genetics, 2020Co-Authors: Christa E Moore, John M ArchibaldAbstract:Nucleomorphs are the remnant nuclei of algal endosymbionts in cryptophytes and Chlorarachniophytes, two evolutionarily distinct unicellular eukaryotic lineages that acquired photosynthesis secondarily by the engulfment of red and green algae, respectively. At less than one million base pairs in size, nucleomorph genomes are the most highly reduced nuclear genomes known, with three small linear chromosomes and a gene density similar to that seen in prokaryotes. The independent origin of nucleomorphs in cryptophytes and Chlorarachniophytes presents an interesting opportunity to study the reductive evolutionary forces that have led to their remarkable convergence upon similar genome architectures and coding capacities. In this article, we review the current state of knowledge with respect to the structure, function, origin, and evolution of nucleomorph genomes across the known diversity of cryptophyte and Chlorarachniophyte algae.
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Nucleomorph Small RNAs in Cryptophyte and Chlorarachniophyte Algae
Genome Biology and Evolution, 2019Co-Authors: Anna K M Åsman, Bruce A Curtis, John M ArchibaldAbstract:The regulation of gene expression and RNA maturation underlies fundamental processes such as cell homeostasis, development, and stress acclimation. The biogenesis and modification of RNA is tightly controlled by an array of regulatory RNAs and nucleic acid-binding proteins. While the role of small RNAs (sRNAs) in gene expression has been studied in-depth in select model organisms, little is known about sRNA biology across the eukaryotic tree of life. We used deep sequencing to explore the repertoires of sRNAs encoded by the miniaturized, endosymbiotically derived "nucleomorph" genomes of two single-celled algae, the cryptophyte Guillardia theta and the Chlorarachniophyte Bigelowiella natans. A total of 32.3 and 35.3 million reads were generated from G. theta and B. natans, respectively. In G. theta, we identified nucleomorph U1, U2, and U4 spliceosomal small nuclear RNAs (snRNAs) as well as 11 C/D box small nucleolar RNAs (snoRNAs), five of which have potential plant and animal homologs. The snoRNAs are predicted to perform 2'-O methylation of rRNA (but not snRNA). In B. natans, we found the previously undetected 5S rRNA as well as six orphan sRNAs. Analysis of Chlorarachniophyte snRNAs shed light on the removal of the miniature 18-21 nt introns found in B. natans nucleomorph genes. Neither of the nucleomorph genomes appears to encode RNA pseudouridylation machinery, and U5 snRNA cannot be found in the cryptophyte G. theta. Considering the central roles of U5 snRNA and RNA modifications in other organisms, cytoplasm-to-nucleomorph RNA shuttling in cryptophyte algae is a distinct possibility.
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Relative Mutation Rates in Nucleomorph-Bearing Algae
Genome Biology and Evolution, 2019Co-Authors: Cameron J. Grisdale, David Roy Smith, John M ArchibaldAbstract:Chlorarachniophyte and cryptophyte algae are unique among plastid-containing species in that they have a nucleomorph genome: a compact, highly reduced nuclear genome from a photosynthetic eukaryotic endosymbiont. Despite their independent origins, the nucleomorph genomes of these two lineages have similar genomic architectures, but little is known about the evolutionary pressures impacting nucleomorph DNA, particularly how their rates of evolution compare to those of the neighboring genetic compartments (the mitochondrion, plastid, and nucleus). Here, we use synonymous substitution rates to estimate relative mutation rates in the four genomes of nucleomorph-bearing algae. We show that the relative mutation rates of the host versus endosymbiont nuclear genomes are similar in both Chlorarachniophytes and cryptophytes, despite the fact that nucleomorph gene sequences are notoriously highly divergent. There is some evidence, however, for slightly elevated mutation rates in the nucleomorph DNA of Chlorarachniophytes-a feature not observed in that of cryptophytes. For both lineages, relative mutation rates in the plastid appear to be lower than those in the nucleus and nucleomorph (and, in one case, the mitochondrion), which is consistent with studies of other plastid-bearing protists. Given the divergent nature of nucleomorph genes, our finding of relatively low evolutionary rates in these genomes suggests that for both lineages a burst of evolutionary change and/or decreased selection pressures likely occurred early in the integration of the secondary endosymbiont.
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Ubiquitin fusion proteins in algae: implications for cell biology and the spread of photosynthesis
BMC Genomics, 2019Co-Authors: Shannon J. Sibbald, Julia F Hopkins, Gina V. Filloramo, John M ArchibaldAbstract:Background The process of gene fusion involves the formation of a single chimeric gene from multiple complete or partial gene sequences. Gene fusion is recognized as an important mechanism by which genes and their protein products can evolve new functions. The presence-absence of gene fusions can also be useful characters for inferring evolutionary relationships between organisms. Results Here we show that the nuclear genomes of two unrelated single-celled algae, the cryptophyte Guillardia theta and the Chlorarachniophyte Bigelowiella natans , possess an unexpected diversity of genes for ubiquitin fusion proteins, including novel arrangements in which ubiquitin occupies amino-terminal, carboxyl-terminal, and internal positions relative to its fusion partners. We explore the evolution of the ubiquitin multigene family in both genomes, and show that both algae possess a gene encoding an ubiquitin-nickel superoxide dismutase fusion protein (Ubiq-NiSOD) that is widely but patchily distributed across the eukaryotic tree of life – almost exclusively in phototrophs. Conclusion Our results suggest that ubiquitin fusion proteins are more common than currently appreciated; because of its small size, the ubiquitin coding region can go undetected when gene predictions are carried out in an automated fashion. The punctate distribution of the Ubiq-NiSOD fusion across the eukaryotic tree could serve as a beacon for the spread of plastids from eukaryote to eukaryote by secondary and/or tertiary endosymbiosis.
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Ubiquitin fusion proteins in algae: implications for cell biology and the spread of photosynthesis
BMC Genomics, 2019Co-Authors: Shannon J. Sibbald, Julia F Hopkins, Gina V. Filloramo, John M ArchibaldAbstract:The process of gene fusion involves the formation of a single chimeric gene from multiple complete or partial gene sequences. Gene fusion is recognized as an important mechanism by which genes and their protein products can evolve new functions. The presence-absence of gene fusions can also be useful characters for inferring evolutionary relationships between organisms. Here we show that the nuclear genomes of two unrelated single-celled algae, the cryptophyte Guillardia theta and the Chlorarachniophyte Bigelowiella natans, possess an unexpected diversity of genes for ubiquitin fusion proteins, including novel arrangements in which ubiquitin occupies amino-terminal, carboxyl-terminal, and internal positions relative to its fusion partners. We explore the evolution of the ubiquitin multigene family in both genomes, and show that both algae possess a gene encoding an ubiquitin-nickel superoxide dismutase fusion protein (Ubiq-NiSOD) that is widely but patchily distributed across the eukaryotic tree of life – almost exclusively in phototrophs. Our results suggest that ubiquitin fusion proteins are more common than currently appreciated; because of its small size, the ubiquitin coding region can go undetected when gene predictions are carried out in an automated fashion. The punctate distribution of the Ubiq-NiSOD fusion across the eukaryotic tree could serve as a beacon for the spread of plastids from eukaryote to eukaryote by secondary and/or tertiary endosymbiosis.
Patrick J Keeling - One of the best experts on this subject based on the ideXlab platform.
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Extensive Reduction of the Nuclear Pore Complex in Nucleomorphs
Genome Biology and Evolution, 2019Co-Authors: Nicholas A. T. Irwin, Patrick J KeelingAbstract:The nuclear pore complex (NPC) is a large macromolecular assembly situated within the pores of the nuclear envelope. Through interactions between its subcomplexes and import proteins, the NPC mediates the transport of molecules into and out of the nucleus and facilitates dynamic chromatin regulation and gene expression. Accordingly, the NPC constitutes a highly integrated nuclear component that is ubiquitous and conserved among eukaryotes. Potential exceptions to this are nucleomorphs: Highly reduced, relict nuclei that were derived from green and red algae following their endosymbiotic integration into two lineages, the Chlorarachniophytes and the cryptophyceans. A previous investigation failed to identify NPC genes in nucleomorph genomes suggesting that these genes have either been relocated to the host nucleus or lost. Here, we sought to investigate the composition of the NPC in nucleomorphs by using genomic and transcriptomic data to identify and phylogenetically classify NPC proteins in nucleomorph-containing algae. Although we found NPC proteins in all examined lineages, most of those found in Chlorarachniophytes and cryptophyceans were single copy, host-related proteins that lacked signal peptides. Two exceptions were Nup98 and Rae1, which had clear nucleomorph-derived homologs. However, these proteins alone are likely insufficient to structure a canonical NPC and previous reports revealed that Nup98 and Rae1 have other nuclear functions. Ultimately, these data indicate that nucleomorphs represent eukaryotic nuclei without a canonical NPC, raising fundamental questions about their structure and function.
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Letter OverexpressionofMolecularChaperoneGenesinNucleomorph Genomes
2014Co-Authors: Yoshihisa Hirakawa, John M Archibald, Shigekatsu Suzuki, Patrick J Keeling, Ken-ichiro IshidaAbstract:Chlorarachniophytes and cryptophytes possess complex plastids that were acquired by the ingestion of a green and red algal endosymbiont, respectively. The plastids are surrounded by four membranes, and a relict nucleus, called the nucleomorph, remains in the periplastidal compartment, which corresponds to the remnant cytoplasm of the endosymbiont. Nucleomorphs contain a greatly reduced genome that possesses only several hundred genes with high evolutionary rates. We examined the relative transcription levels of the genes of all proteins encoded by the nucleomorph genomes of two Chlorarachniophytes and three cryptophytes using an RNA-seq transcriptomic approach. The genes of two heat shock proteins, Hsp70 and Hsp90, were highly expressed under normal conditions. It has been shown that molecular chaperone overexpression allows an accumulation of genetic mutations in bacteria. Our results suggest that overexpression of heat shock proteins in nucleomorph genomes may play a role in buffering the mutational destabilization of proteins, which might allow the high evolutionary rates of nucleomorph-encoded proteins.
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Dual targeting of aminoacyl-tRNA synthetases to the mitochondrion and complex plastid in Chlorarachniophytes.
Journal of Cell Science, 2012Co-Authors: Yoshihisa Hirakawa, Fabien Burki, Patrick J KeelingAbstract:Summary In plants, many nucleus-encoded proteins are targeted to both mitochondria and plastids, and this process is generally mediated by ambiguous N-terminal targeting sequences that are recognized by receptors on both organelles. In many algae, however, plastids were acquired by secondarily engulfing green or red algae, which were retained within the endomembrane system. Protein targeting to these secondary plastids is more complex, and because they do not reside directly in the cytoplasm, dual targeting cannot function as it does in plant cells. Here we investigate dual targeting of aminoacyl-tRNA synthetases (aaRSs) in Chlorarachniophytes, which are complex algae that possess secondary plastids and a relict nucleus derived from a green algal endosymbiont. Chlorarachniophytes have four genome-containing compartments, but almost all the aaRSs are nucleus-encoded and present in fewer than four copies (some as few as two), suggesting multiple targeting. We characterized the subcellular localization of two classes, HisRS (three copies) and GlyRS (two copies), using GFP fusion proteins. In both cases, one copy was dually targeted to mitochondria and plastids, but unlike plants this was mediated by translation initiation variants. We also found that the periplastidal compartment (the relict green algal cytoplasm) lacks both GlyRS and a cognate tRNA, suggesting that pre-charged host tRNAs are imported into this compartment. Leader analysis of other aaRSs suggests that alternative translation is a common strategy for dual targeting in these complex cells. Overall, dual targeting to mitochondria and plastids is a shared feature of plastid-bearing organisms, but the increased complexity of trafficking into secondary plastids requires a different strategy.
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genome based reconstruction of the protein import machinery in the secondary plastid of a Chlorarachniophyte alga
Eukaryotic Cell, 2012Co-Authors: Yoshihisa Hirakawa, Fabien Burki, Patrick J KeelingAbstract:ABSTRACT Most plastid proteins are encoded by their nuclear genomes and need to be targeted across multiple envelope membranes. In vascular plants, the translocons at the outer and inner envelope membranes of chloroplasts (TOC and TIC, respectively) facilitate transport across the two plastid membranes. In contrast, several algal groups harbor more complex plastids, the so-called secondary plastids, which are surrounded by three or four membranes, but the plastid protein import machinery (in particular, how proteins cross the membrane corresponding to the secondary endosymbiont plasma membrane) remains unexplored in many of these algae. To reconstruct the putative protein import machinery of a secondary plastid, we used the Chlorarachniophyte alga Bigelowiella natans, whose plastid is bounded by four membranes and still possesses a relict nucleus of a green algal endosymbiont (the nucleomorph) in the intermembrane space. We identified nine homologs of plant-like TOC/TIC components in the recently sequenced B. natans nuclear genome, adding to the two that remain in the nucleomorph genome (B. natans TOC75 [BnTOC75] and BnTIC20). All of these proteins were predicted to be localized to the plastid and might function in the inner two membranes. We also show that the homologs of a protein, Der1, that is known to mediate transport across the second membrane in the several lineages with secondary plastids of red algal origin is not associated with plastid protein targeting in B. natans. How plastid proteins cross this membrane remains a mystery, but it is clear that the protein transport machinery of Chlorarachniophyte plastids differs from that of red algal secondary plastids.
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morphological diversity between culture strains of a Chlorarachniophyte lotharella globosa
PLOS ONE, 2011Co-Authors: Yoshihisa Hirakawa, Alexis Howe, Erick R James, Patrick J KeelingAbstract:Chlorarachniophytes are marine unicellular algae that possess secondary plastids of green algal origin. Although Chlorarachniophytes are a small group (the phylum of Chlorarachniophyta contains 14 species in 8 genera), they have variable and complex life cycles that include amoeboid, coccoid, and/or flagellate cells. The majority of Chlorarachniophytes possess two or more cell types in their life cycles, and which cell types are found is one of the principle morphological criteria used for species descriptions. Here we describe an unidentified Chlorarachniophyte that was isolated from an artificial coral reef that calls this criterion into question. The life cycle of the new strain includes all three major cell types, but DNA barcoding based on the established nucleomorph ITS sequences showed it to share 100% sequence identity with Lotharella globosa. The type strain of L. globosa was also isolated from a coral reef, but is defined as completely lacking an amoeboid stage throughout its life cycle. We conclude that L. globosa possesses morphological diversity between culture strains, and that the new strain is a variety of L. globosa, which we describe as Lotharella globosa var. fortis var. nov. to include the amoeboid stage in the formal description of L. globosa. This intraspecies variation suggest that gross morphological stages maybe lost rather rapidly, and specifically that the type strain of L. globosa has lost the ability to form the amoeboid stage, perhaps recently. This in turn suggests that even major morphological characters used for taxonomy of this group may be variable in natural populations, and therefore misleading.
Yoshihisa Hirakawa - One of the best experts on this subject based on the ideXlab platform.
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Chlorarachniophytes With Complex Secondary Plastids of Green Algal Origin
Advances in Botanical Research, 2017Co-Authors: Yoshihisa HirakawaAbstract:Abstract Diverse algae have evolved ‘secondary’ plastids through parallel endosymbiotic uptakes of photosynthetic eukaryotes either of green or red algae, and these events are referred to as secondary endosymbioses. Chlorarachniophytes are a group of marine unicellular algae with four-membrane-bound secondary plastids that originated from a green algal endosymbiont. Remarkably, Chlorarachniophyte plastids possess a vestigial nucleus termed a ‘nucleomorph’ in the periplastidal compartment between the second and third membranes that corresponds to the remnant cytoplasm of the endosymbiont. Given that endosymbiont nuclei have disappeared in most secondary plastid-bearing algae, Chlorarachniophytes appear to represent an intermediate stage of secondary endosymbiosis and thereby offer an interesting opportunity to study complex plastid evolution. In this chapter, I summarise the current understanding of the evolutionary history of Chlorarachniophytes in terms of morphology, phylogeny, and genomics.
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diurnal transcriptional regulation of endosymbiotically derived genes in the Chlorarachniophyte bigelowiella natans
Genome Biology and Evolution, 2016Co-Authors: Shigekatsu Suzuki, Ken-ichiro Ishida, Yoshihisa HirakawaAbstract:Chlorarachniophyte algae possess complex plastids acquired by the secondary endosymbiosis of a green alga, and the plastids harbor a relict nucleus of the endosymbiont, the so-called nucleomorph. Due to massive gene transfer from the endosymbiont to the host, many proteins involved in plastid and nucleomorph are encoded by the nuclear genome. Genome sequences have provided a blueprint for the fate of endosymbiotically derived genes; however, transcriptional regulation of these genes remains poorly understood. To gain insight into the evolution of endosymbiotic genes, we performed genome-wide transcript profiling along the cell cycle of the Chlorarachniophyte Bigelowiella natans, synchronized by light and dark cycles. Our comparative analyses demonstrated that transcript levels of 7,751 nuclear genes (35.7% of 21,706 genes) significantly oscillated along the diurnal/cell cycles, and those included 780 and 147 genes for putative plastid and nucleomorph-targeted proteins, respectively. Clustering analysis of those genes revealed the existence of transcriptional networks related to specific biological processes such as photosynthesis, carbon metabolism, translation, and DNA replication. Interestingly, transcripts of many plastid-targeted proteins in B. natans were induced before dawn, unlike other photosynthetic organisms. In contrast to nuclear genes, 99% nucleomorph genes were found to be constitutively expressed during the cycles. We also found that the nucleomorph DNA replication would be controlled by a nucleus-encoded viral-like DNA polymerase. The results of this study suggest that nucleomorph genes have lost transcriptional regulation along the diurnal cycles, and nuclear genes exert control over the complex plastid including the nucleomorph.
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Plastid genome sequences of Gymnochlora stellata, Lotharella vacuolata, and Partenskyella glossopodia reveal remarkable structural conservation among Chlorarachniophyte species
Journal of Plant Research, 2016Co-Authors: Shigekatsu Suzuki, Yoshihisa Hirakawa, Rumiko Kofuji, Mamoru Sugita, Ken-ichiro IshidaAbstract:Chlorarachniophyte algae have complex plastids acquired by the uptake of a green algal endosymbiont, and this event is called secondary endosymbiosis. Interestingly, the plastids possess a relict endosymbiont nucleus, referred to as the nucleomorph, in the intermembrane space, and the nucleomorphs contain an extremely reduced and compacted genome in comparison with green algal nuclear genomes. Therefore, Chlorarachniophyte plastids consist of two endosymbiotically derived genomes, i.e., the plastid and nucleomorph genomes. To date, complete nucleomorph genomes have been sequenced in four different species, whereas plastid genomes have been reported in only two species in Chlorarachniophytes. To gain further insight into the evolution of endosymbiotic genomes in Chlorarachniophytes, we newly sequenced the plastid genomes of three species, Gymnochlora stellata , Lotharella vacuolata , and Partenskyella glossopodia . Our findings reveal that Chlorarachniophyte plastid genomes are highly conserved in size, gene content, and gene order among species, but their nucleomorph genomes are divergent in such features. Accordingly, the current architecture of the plastid genomes of Chlorarachniophytes evolved in a common ancestor, and changed very little during their subsequent diversification. Furthermore, our phylogenetic analyses using multiple plastid genes suggest that Chlorarachniophyte plastids are derived from a green algal lineage that is closely related to Bryopsidales in the Ulvophyceae group.
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prospective function of ftsz proteins in the secondary plastid of Chlorarachniophyte algae
BMC Plant Biology, 2015Co-Authors: Yoshihisa Hirakawa, Ken-ichiro IshidaAbstract:Division of double-membraned plastids (primary plastids) is performed by constriction of a ring-like division complex consisting of multiple plastid division proteins. Consistent with the endosymbiotic origin of primary plastids, some of the plastid division proteins are descended from cyanobacterial cell division machinery, and the others are of host origin. In several algal lineages, complex plastids, the “secondary plastids”, have been acquired by the endosymbiotic uptake of primary plastid-bearing algae, and are surrounded by three or four membranes. Although homologous genes for primary plastid division proteins have been found in genome sequences of secondary plastid-bearing organisms, little is known about the function of these proteins or the mechanism of secondary plastid division. To gain insight into the mechanism of secondary plastid division, we characterized two plastid division proteins, FtsZD-1 and FtsZD-2, in Chlorarachniophyte algae. FtsZ homologs were encoded by the nuclear genomes and carried an N-terminal plastid targeting signal. Immunoelectron microscopy revealed that both FtsZD-1 and FtsZD-2 formed a ring-like structure at the midpoint of bilobate plastids with a projecting pyrenoid in Bigelowiella natans. The ring was always associated with a shallow plate-like invagination of the two innermost plastid membranes. Furthermore, gene expression analysis confirmed that transcripts of ftsZD genes were periodically increased soon after cell division during the B. natans cell cycle, which is not consistent with the timing of plastid division. Our findings suggest that Chlorarachniophyte FtsZD proteins are involved in partial constriction of the inner pair of plastid membranes, but not in the whole process of plastid division. It is uncertain how the outer pair of plastid membranes is constricted, and as-yet-unknown mechanism is required for the secondary plastid division in Chlorarachniophytes.
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Nucleomorph Genome Sequences of Two Chlorarachniophytes, Amorphochlora amoebiformis and Lotharella vacuolata.
Genome Biology and Evolution, 2015Co-Authors: Shigekatsu Suzuki, Yoshihisa Hirakawa, Shu Shirato, Ken-ichiro IshidaAbstract:Many algal groups acquired complex plastids by the uptake of green and red algae through multiple secondary endosymbioses. As a result of gene loss and transfer during the endosymbiotic processes, algal endosymbiont nuclei disappeared in most cases. However, Chlorarachniophytes and cryptophytes still possess a relict nucleus, so-called the nucleomorph, of the green and red algal endosymbiont, respectively. Nucleomorph genomes are an interesting and suitable model to study the reductive evolution of endosymbiotically derived genomes. To date, nucleomorph genomes have been sequenced in four cryptophyte species and two Chlorarachniophyte species, including Bigelowiella natans (373 kb) and Lotharella oceanica (610 kb). In this study, we report complete nucleomorph genome sequences of two Chlorarachniophytes, Amorphochlora amoebiformis and Lotharella vacuolata, to gain insight into the reductive evolution of nucleomorph genomes in the Chlorarachniophytes. The nucleomorph genomes consist of three chromosomes totaling 374 and 432 kb in size in A. amoebiformis and L. vacuolata, respectively. Comparative analyses among four Chlorarachniophyte nucleomorph genomes revealed that these sequences share 171 function-predicted genes (86% of total 198 function-predicted nucleomorph genes), including the same set of genes encoding 17 plastid-associated proteins, and no evidence of a recent nucleomorph-to-nucleus gene transfer was found. This suggests that Chlorarachniophyte nucleomorph genomes underwent most of their reductive evolution prior to the radiation of extent members of the group. However, there are slight variations in genome size, GC content, duplicated gene number, and subtelomeric regions among the four nucleomorph genomes, suggesting that the genomes might be undergoing changes that do not affect the core functions in each species.
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the complete chloroplast genome of the Chlorarachniophyte bigelowiella natans evidence for independent origins of Chlorarachniophyte and euglenid secondary endosymbionts
Molecular Biology and Evolution, 2007Co-Authors: Matthew B. Rogers, Geoffrey I. Mcfadden, Paul R. Gilson, Vanessa Su, Patrick J KeelingAbstract:Chlorarachniophytes are amoeboflagellate cercozoans that acquired a plastid by secondary endosymbiosis. Chlorarachniophytes are the last major group of algae for which there is no completely sequenced plastid genome. Here we describe the 69.2-kbp chloroplast genome of the model Chlorarachniophyte Bigelowiella natans. The genome is highly reduced in size compared with plastids of other photosynthetic algae and is closer in size to genomes of several nonphotosynthetic plastids. Unlike nonphotosynthetic plastids, however, the B. natans chloroplast genome has not sustained a massive loss of genes, and it retains nearly all of the functional photosynthesis-related genes represented in the genomes of other green algae. Instead, the genome is highly compacted and gene dense. The genes are organized with a strong strand bias, and several unusual rearrangements and inversions also characterize the genome; notably, an inversion in the small-subunit rRNA gene, a translocation of 3 genes in the major ribosomal protein operon, and the fragmentation of the cluster encoding the large photosystem proteins PsaA and PsaB. The chloroplast endosymbiont is known to be a green alga, but its evolutionary origin and relationship to other primary and secondary green plastids has been much debated. A recent hypothesis proposes that the endosymbionts of Chlorarachniophytes and euglenids share a common origin (the Cabozoa hypothesis). We inferred phylogenies using individual and concatenated gene sequences for all genes in the genome. Concatenated gene phylogenies show a relationship between the B. natans plastid and the ulvophyte-trebouxiophyte-chlorophyte clade of green algae to the exclusion of Euglena. The B. natans plastid is thus not closely related to that of Euglena, which suggests that plastids originated independently in these 2 groups and the Cabozoa hypothesis is false.
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complete nucleotide sequence of the Chlorarachniophyte nucleomorph nature s smallest nucleus
Proceedings of the National Academy of Sciences of the United States of America, 2006Co-Authors: Paul R. Gilson, Patrick J Keeling, Claudio H. Slamovits, Vanessa Su, Michael Reith, Geoffrey I. McfaddenAbstract:The introduction of plastids into different heterotrophic protists created lineages of algae that diversified explosively, proliferated in marine and freshwater environments, and radically altered the biosphere. The origins of these secondary plastids are usually inferred from the presence of additional plastid membranes. However, two examples provide unique snapshots of secondary-endosymbiosis-in-action, because they retain a vestige of the endosymbiont nucleus known as the nucleomorph. These are Chlorarachniophytes and cryptomonads, which acquired their plastids from a green and red alga respectively. To allow comparisons between them, we have sequenced the nucleomorph genome from the Chlorarachniophyte Bigelowiella natans: at a mere 373,000 bp and with only 331 genes, the smallest nuclear genome known and a model for extreme reduction. The genome is eukaryotic in nature, with three linear chromosomes containing densely packed genes with numerous overlaps. The genome is replete with 852 introns, but these are the smallest introns known, being only 18, 19, 20, or 21 nt in length. These pygmy introns are shown to be miniaturized versions of normal-sized introns present in the endosymbiont at the time of capture. Seventeen nucleomorph genes encode proteins that function in the plastid. The other nucleomorph genes are housekeeping entities, presumably underpinning maintenance and expression of these plastid proteins. Chlorarachniophyte plastids are thus serviced by three different genomes (plastid, nucleomorph, and host nucleus) requiring remarkable coordination and targeting. Although originating by two independent endosymbioses, Chlorarachniophyte and cryptomonad nucleomorph genomes have converged upon remarkably similar architectures but differ in many molecular details that reflect two distinct trajectories to hypercompaction and reduction.
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Jam packed genomes – a preliminary, comparative analysis of nucleomorphs
Genetica, 2002Co-Authors: Paul R. Gilson, Geoffrey I. McfaddenAbstract:There are two ways eukaryotic cells can permanently acquire chloroplasts. They can take up a cyanobacterium and turn it into a chloroplast or they can engulf an alga that already has a chloroplast. The second method is far more common and there are at least seven major groups of protists that have obtained their chloroplasts, this way. In most cases little remains of the engulfed alga apart from its chloroplast, but in two groups, the cryptomonads and Chlorarachniophytes, a small remnant nucleus of the engulfed alga is still present. These tiny nuclei, called nucleomorphs, are the smallest and most compact eukaryotic genomes known and recently the nucleomorph of the cryptomonad alga Guillardia theta , was completely sequenced (551 kilobases). The nucleomorph of the Chlorarachniophyte Bigellowiella natans (380 kilobases), is also being sequenced and is about half complete. We discuss some of the similarities and differences that are emerging between these two nucleomorph genomes. Both genomes contain just three chromosomes that encode mainly housekeeping genes and a few proteins for chloroplast functions. The bulk of nucleomorph gene coding capacity, therefore, appears to be devoted to self perpetuation and creating gene and protein expression machineries to make a small number of essential chloroplast proteins. We discuss reasons why both nucleomorphs are extraordinarily compact and why their gene sequences are evolving rapidly.
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Jam packed genomes-a preliminary, comparative analysis of nucleomorphs
Genetica, 2002Co-Authors: Paul R. Gilson, Geoffrey I. McfaddenAbstract:There are two ways eukaryotic cells can permanently acquire chloroplasts. They can take up a cyanobacterium and turn it into a chloroplast or they can engulf an alga that already has a chloroplast. The second method is far more common and there are at least seven major groups of protists that have obtained their chloroplasts, this way. In most cases little remains of the engulfed alga apart from its chloroplast, but in two groups, the cryptomonads and Chlorarachniophytes, a small remnant nucleus of the engulfed alga is still present. These tiny nuclei, called nucleomorphs, are the smallest and most compact eukaryotic genomes known and recently the nucleomorph of the cryptomonad alga Guillardia theta, was completely sequenced (551 kilobases). The nucleomorph of the Chlorarachniophyte Bigellowiella natans (380 kilobases), is also being sequenced and is about half complete. We discuss some of the similarities and differences that are emerging between these two nucleomorph genomes. Both genomes contain just three chromosomes that encode mainly housekeeping genes and a few proteins for chloroplast functions. The bulk of nucleomorph gene coding capacity, therefore, appears to be devoted to self perpetuation and creating gene and protein expression machineries to make a small number of essential chloroplast proteins. We discuss reasons why both nucleomorphs are extraordinarily compact and why their gene sequences are evolving rapidly.
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Evidence for nucleomorph to host nucleus gene transfer: light-harvesting complex proteins from cryptomonads and Chlorarachniophytes.
Protist, 2000Co-Authors: James A. Deane, Dion G Durnford, Uwe G Maier, Martin Fraunholz, Vanessa Su, William Martin, Geoffrey I. McfaddenAbstract:Summary Cryptomonads and Chlorarachniophytes acquired photosynthesis independently by engulfing and retaining eukaryotic algal cells. The nucleus of the engulfed cells (known as a nucleomorph) is much reduced and encodes only a handful of the numerous essential plastid proteins normally encoded by the nucleus of chloroplast-containing organisms. In cryptomonads and Chlorarachniophytes these proteins are thought to be encoded by genes in the secondary host nucleus. Genes for these proteins were potentially transferred from the nucleomorph (symbiont nucleus) to the secondary host nucleus; nucleus to nucleus intracellular gene transfers. We isolated complementary DNA clones (cDNAs) for chlorophyll-binding proteins from a cryptomonad and a Chlorarachniophyte. In each organism these genes reside in the secondary host nuclei, but phylogenetic evidence, and analysis of the targeting mechanisms, suggest the genes were initially in the respective nucleomorphs (symbiont nuclei). Implications for origins of secondary endosymbiotic algae are discussed.