Diversity of the Photosynthetic Paulinella Species, with the Description of Paulinella micropora sp. nov. and the Chromatophore Genome Sequence for strain KR01

Lhee, Duckhyun; Yang, Eun Chan; Kim, Jong Im; Nakayama, Takuro; Zuccarello, Giuseppe C.; Andersen, Robert A.; Yoon, Hwan Su

doi:10.1016/j.protis.2017.01.003

Cited by 35 publications

(42 citation statements)

References 59 publications

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“…A second primary endosymbiosis has occurred in some species of the testate Rhizarian amoeba Paulinella (Lhee et al, 2017). Photosynthetic Paulinella species acquired photosynthesis and carbon fixation via endosymbiosis of a member of the CSP clade.…”

Section: Resultsmentioning

confidence: 99%

Ferredoxin-dependent bilin reductases in eukaryotic algae: Ubiquity and diversity

Rockwell

Lagarias

2017

Journal of Plant Physiology

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Linear tetrapyrroles (bilins) are produced from heme by heme oxygenase, usually forming biliverdin IXα (BV). Fungi and bacteria use BV as chromophore for phytochrome photoreceptors. Oxygenic photosynthetic organisms use BV as a substrate for ferredoxin-dependent bilin reductases (FDBRs), enzymes that produce diverse reduced bilins used as light-harvesting pigments in phycobiliproteins and as photoactive photoreceptor chromophores. Bilin biosynthesis is essential for phototrophic growth in Chlamydomonas reinhardtii despite the absence of phytochromes or phycobiliproteins in this organism, raising the possibility that bilins are more generally required for phototrophic growth by algae. We here leverage the recent expansion in available algal transcriptomes, cyanobacterial genomes, and environmental metagenomes to analyze the distribution and diversification of FDBRs. With the possible exception of euglenids, FDBRs are present in all photosynthetic eukaryotic lineages. Phylogenetic analysis demonstrates that algal FDBRs belong to the three previously recognized FDBR lineages. Our studies provide new insights into FDBR evolution and diversification.

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Section: Resultsmentioning

confidence: 99%

Ferredoxin-dependent bilin reductases in eukaryotic algae: Ubiquity and diversity

Rockwell

Lagarias

2017

Journal of Plant Physiology

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“…To estimate gene transfer timing, the branching time point when P. micropora MYN1 separated from the nearest non-rhizarian organisms in the ML phylogenetic tree was calculated using the RelTime method 55 . We used an estimated value of the divergence of P. micropora and P. chromatophora (45.7–64.7 MYA) based on the 18S rRNA phylogenetic tree corrected by fossil information 11,60 .…”

Section: Methodsmentioning

confidence: 99%

Large DNA virus promoted the endosymbiotic evolution to make a photosynthetic eukaryote

Matsuo

Katahata

Tachikawa

et al. 2019

Preprint

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Chloroplasts in photosynthetic eukaryotes originated from a cyanobacterial endosymbiosis far more than 1 billion years ago1-3. Due to this ancientness, it remains unclear how this evolutionary process proceeded. To unveil this mystery, we analysed the whole genome sequence of a photosynthetic rhizarian amoeba4, Paulinella micropora5,6, which has a chloroplast-like organelle that originated from another cyanobacterial endosymbiosis7-10 about 0.1 billion years ago11. Here we show that the predacious amoeba that engulfed cyanobacteria evolved into a photosynthetic organism very quickly in the evolutionary time scale, probably aided by the drastic genome reorganization activated by large DNA virus. In the endosymbiotic evolution of eukaryotic cells, gene transfer from the endosymbiont genome to the host nucleus is essential for the evolving host cell to control the endosymbiont-derived organelle12. In P. micropora, we found that the gene transfer from the free-living and endosymbiotic bacteria to the amoeba nucleus was rapidly activated but both simultaneously ceased within the initiation period of the endosymbiotic evolution, suggesting that the genome reorganization drastically proceeded and completed. During this period, large DNA virus appeared to have infected the amoeba, followed by the rapid amplification and diversification of virus-related genes. These findings led us to re-examine the conventional endosymbiotic evolutionary scenario that exclusively deals with the host and the symbiont, and to extend it by incorporating a third critical player, large DNA virus, which activates the drastic gene transfer and genome reorganization between them. This Paulinella version of the evolutionary hypothesis deserves further testing of its generality in evolutionary systems and could shed light on the unknown roles of large DNA viruses13 in the evolution of terrestrial life.

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“…Paulinella micropora KR01 was isolated from a natural freshwater sample collected on August 18, 2009 from Mangae Jeosuji (Reservoir), Chungnam Province, South Korea (see Lhee, et al 2017). We established an uni-algal, axenic culture of KR01 (for details see Supplementary Information Materials and Methods).…”

Section: Sampling Isolation and Dna/ Rna Extractionmentioning

confidence: 99%

“…In contrast to the highly reduced plastid genomes of algae and plants (i.e., 100-200 kbp in size in Archaeplastida), the cyanobacterium-derived plastid (referred to as the chromatophore) in phototrophic Paulinella is in a less derived stage of organelle evolution and is ca. 1 Mbp in size (Lhee, et al 2017;Nowack, et al 2008;Reyes-Prieto, et al 2010;Zhang, et al 2017).…”

Section: Introductionmentioning

confidence: 99%

“…To advance knowledge about primary EGT and genome evolution in photosynthetic Paulinella, we generated a draft genome assembly and transcriptome data from Paulinella micropora strain KR01 (hereafter, KR01; Lhee, et al 2017), as well as complete or nearcomplete draft genomes from four co-cultured bacteria. These data comprise a valuable reference platform for studying the origin and integration of the chromatophore in this independent case of plastid primary origin.…”

Section: Introductionmentioning

confidence: 99%

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Paulinella micropora KR01 holobiont genome assembly for studying primary plastid evolution

Lhee

Lee

Cho

et al. 2019

Preprint

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The widespread algal and plant (Archaeplastida) plastid originated >1 billion years ago, therefore relatively little can be learned about plastid integration during the initial stages of primary endosymbiosis by studying these highly derived species. Here we focused on a unique model for endosymbiosis research, the photosynthetic amoeba Paulinella micropora KR01 (Rhizaria) that underwent a more recent independent primary endosymbiosis about 124 Mya. A total of 149 Gbp of PacBio and 19 Gbp of Illumina data were used to generate the draft assembly that comprises 7,048 contigs with N50=143,028 bp and a total length of 707Mbp. Genome GC-content was 44% with 76% repetitive sequences. We predicted 32,358 genes that contain 73% of the complete, conserved genes in the BUSCO database. The mean intron length was 882 bp, which is significantly greater than in other Rhizaria (86~184 bp).Symbiotic bacteria from the culture were isolated and completed genomes were generated from three species (Mesorhizobium amorphae Pch-S, Methylibium petroeiphilum Pch-M, Polaromonas sp. Pch-P) with one draft genome (Pimelobacter simplex Pch-N). Our holobiont data establish P. micropora KR01 as a model for studying plastid integration and the role of bacterial symbionts in Paulinella biology.

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Diversity of the Photosynthetic Paulinella Species, with the Description of Paulinella micropora sp. nov. and the Chromatophore Genome Sequence for strain KR01

Cited by 35 publications

References 59 publications

Ferredoxin-dependent bilin reductases in eukaryotic algae: Ubiquity and diversity

Ferredoxin-dependent bilin reductases in eukaryotic algae: Ubiquity and diversity

Large DNA virus promoted the endosymbiotic evolution to make a photosynthetic eukaryote

Paulinella micropora KR01 holobiont genome assembly for studying primary plastid evolution

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