10, e1003537, https://doi.org/10.1371/journal.pcbi.1003537 (2014). Moran, N. A. Nucleotide substitution and insertion/deletion events were analyzed between P. micropora NZ27 and KR01 strains. Using a capillary pipet, each cell was individually isolated and washed several times with sterile DY-V medium. The orthologous genes were clustered using OrthoFinder71 and alignment was done using MAFFT v7.305b72. The amount of fatty acids in each acyl lipid is shown on the basis of chlorophyll content measured by the amount of phytol. The origin of 15:0 is currently unclear because the resolution of argentation TLC was insufficient to identify this fatty acid, which has an odd number of carbons. . Acad. The extract was dried with solid anhydrous sodium sulfate and evaporated to dryness. Gene expression levels influence amino acid usage and evolutionary rates in endosymbiotic bacteria. A mitochondrial condensing enzyme (type II) was identified in P. chromatophora by a BLAST search using bacterial FabF sequences as queries, as described earlier. (B) Autoradiogram of a part of TLC plate in experiment 2. Gil, R. et al. 59, 537544 (1895). & Moya, A. Tempo and mode of early gene loss in endosymbiotic bacteria from insects. Nevertheless, the time-dependent changes in radioactivity from GlcDG to MGDG were similar to those reported previously in cyanobacteria. Red algal plastids contained more OGFs in other metabolic pathways when compared to its two sister taxa. Lipid analysis of P. micropora. To investigate the history of chromatophore genome reduction, we constructed OGFs from chromatophore proteins and from phylogenetically closely related Synechococcus/Prochlorococcus species. It is not colored membrane associated physical that contained Big Man's. That's difficult. Nomura, M., Nakayama, T. & Ishida, K.-i Detailed process of shell construction in the photosynthetic testate amoeba Paulinella chromatophora (Euglyphid, Rhizaria). PubMed Moreover, chromatophore genomes are much larger than Archaeplastida plastids (see Fig. Figure7B shows the turnover rate of fatty acids in individual lipid classes as calculated from the proportion of labeled molecules. Briefly, P. micropora cells were harvested from 1,600ml of culture, suspended in the grinding buffer, broken by two passages through a French pressure cell (600kg cm2) and fractionated on a Percoll density gradient. D.L. The other group, consisting of phospholipids and DGCC, is likely to be extra-chromatophore lipids and contains fatty acids with longer carbon chains and polyunsaturated fatty acids. (A, C) Argentation TLC. This fatty acid is likely to be synthesized in the ER, by lipid-linked aerobic desaturation of glycerolipids because of its low rate of labeling (Fig. Search for other works by this author on: Present address: Research Center for Functional Materials, National Institute for Materials Science, 1-1 Namiki, Tsukuba, Ibaraki, 305-0044 Japan. Hidden in the shadows is a cornucopia of mostly single-celled organisms called the protists that are revealing new biological insights and giving us a more complete understanding of ecosystems and climate change. Mass spectral data were processed using C13DIST software (Sato etal. 42, 165190, https://doi.org/10.1146/annurev.genet.41.110306.130119 (2008). Among these, 584 OGFs, with some additional orthologs were examined in detail (Fig. is poor in electron-dense materials, but some filaments that we call IntL (possibly polysaccharides) are present. Other principal components were DGDG, PG and PE; PI, PA and unknown lipid X were minor components. FabF sequences (type II condensing enzymes) of bacteria and organelles were retrieved from cluster 111 of Gclust2012_42 and cluster 160 of Gclust2017R (http://gclust.c.u-tokyo.ac.jp/) (Sato 2009). 50 Million years of genomic stasis in endosymbiotic bacteria. The total amount of radioactivity increased during the chase, suggesting that the metabolic intermediates that were labeled during the first 10min photosynthesis were used to synthesize fatty acids during the chase period. PubMed Central USA 100, 93889393, https://doi.org/10.1073/pnas.1533499100 (2003). Various isomers of hexadecenoic acid (16:1) were found, namely, 6, 9 and 11. Find important definitions, questions, meanings, examples, exercises and tests below for In a cyanobacteria the photosynthetic pigments are found is?1 . The thecate amoeba Paulinella is a valuable model for understanding plastid organellogenesis because this lineage has independently gained plastids (termed chromatophores) of alpha-cyanobacterial provenance. This result suggests that AT-enrichment is an ongoing process in chromatophore genomes. Edgar, R. C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. S7) showed that chromatophores synthesized mainly 14:0:16:0 and likely also 15:0 were minor products. Published: June 8, 2023 Updated: June 8, 2023. Among these, only 22 OGFs had intensified selection, whereas the remainder (303 OGFs) showed relaxed selection in chromatophore genes. Moran, N. A. Microbial minimalism: genome reduction in bacterial pathogens. When comparing genomes of endosymbiont lineages, rearrangement and gene content comparisons should be considered in the context of their divergence time. This is evident in the fatty acid composition of lipids, which are classified into two groups. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. 18:2(9,12) for linoleic acid. The thecate amoeba Paulinella is a valuable model for understanding plastid organellogenesis because this lineage has independently gained plastids (termed chromatophores) of alpha-cyanobacterial . 61, 317321, https://doi.org/10.1111/jeu.12102 (2014). These values in this figure were re-calculated from the data in Fig. Free cholesterol was present at a comparable level to these. Curiously, 18:1(9) was detected in TAG. Each tick indicates genes present in the OGFs; red indicates red algae, green are green lineage species, cyan indicates glaucophytes, pink indicates Paulinella, and blue indicates cyanobacteria. (1957/, Yoshitomi T., Kaminaga S., Sato N., Toyoshima M., Moriyama T., Yoshimoto K. (, Oxford University Press is a department of the University of Oxford. TR9), A phylogenetically novel cyanobacterium most closely related to Gloeobacter, Pyropia yezoensis genome reveals diverse mechanisms of carbon acquisition in the intertidal environment, Nucleotide substitution rates of diatom plastid encoded protein genes are positively correlated with genome architecture, https://doi.org/10.1146/annurev.genet.41.110306.130134, https://doi.org/10.1146/annurev-arplant-050312-120144, https://doi.org/10.1371/currents.tol.e68a099364bb1a1e129a17b4e06b0c6b, https://doi.org/10.1111/j.1550-7408.2012.00644.x, https://doi.org/10.1111/j.1550-7408.1995.tb01541.x, https://doi.org/10.1016/j.protis.2005.09.001, https://doi.org/10.1016/j.cub.2006.08.018, https://doi.org/10.1016/j.protis.2017.01.003, https://doi.org/10.1016/j.protis.2015.11.003, https://doi.org/10.1016/j.cub.2008.02.051, https://doi.org/10.1016/j.cub.2017.08.010, https://doi.org/10.1016/S0092-8674(02)00665-7, https://doi.org/10.1146/annurev-micro-091213-112901, https://doi.org/10.1111/j.1365-294X.2008.03912.x, https://doi.org/10.1038/s41559-017-0237-0, https://doi.org/10.1080/10635150490264842, https://doi.org/10.1007/s00792-008-0141-2, https://doi.org/10.1111/j.1469-8137.2010.03195.x, https://doi.org/10.1186/s12915-016-0299-5, https://doi.org/10.1111/j.1759-6831.2012.00237.x, https://doi.org/10.1016/j.bbalip.2016.10.006, https://doi.org/10.1038/nmicrobiol.2016.214, https://doi.org/10.1016/j.gene.2005.04.003, https://doi.org/10.1146/annurev.genet.41.110306.130119, https://doi.org/10.1186/gb-2001-2-12-research0054, https://doi.org/10.1016/0027-5107(64)90047-8, https://doi.org/10.1007/s10709-006-9007-7, https://doi.org/10.1007/s11103-011-9777-x, https://doi.org/10.1371/journal.pgen.1001115, https://doi.org/10.1016/S0168-9525(01)02447-7, https://doi.org/10.1186/s13059-015-0721-2, https://doi.org/10.1093/bioinformatics/bts440, https://doi.org/10.1016/j.jmb.2015.11.006, https://doi.org/10.1093/bioinformatics/btq315, https://doi.org/10.1534/genetics.113.152025, https://doi.org/10.1371/journal.pcbi.1003537, http://creativecommons.org/licenses/by/4.0/. Light harvesting in purple bacteria is performed mainly by three pigment-protein . The presence of TAG and a high level of cholesterol were consistent with the presence of lipid droplets within the cell (Fig. 2C suggests that the lipids are classified into two groups, one including MGDG, DGDG and SQDG and the other including phospholipids, DGCC and TAG. You are using a browser version with limited support for CSS. They are present in various creatures, including fish, amphibians, reptiles, crabs, and cephalopods. (, Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. Sci. Mutat. That is, the impact of selection and codon usage bias in ancestral free-living cyanobacteria are broadly applicable to (and conserved) in captured endosymbiont genomes. The ortholog of this oxidoreductase was pyridoxal reductase involved in vitamin B6 metabolism63,64. Annu. Provided by the Springer Nature SharedIt content-sharing initiative. The observation of relaxed selection on chromatophore genes when compared to free-living alpha-cyanobacteria may, therefore, be explained by the homogeneous intracellular environment. Heatmap with genomes of chromatophores, cyanobacteria, and Archaeplastida plastids categorized by KEGG pathways annotated as Orthologous Gene Families (OGFs). Paulinella longichromatophora was collected from Gomso Bay on the western coast of Korea (35 3111.40N, 126 290.65E) on March 8, 2015. Lipopolysaccharides are large molecules present in the outer membrane of Gram-negative bacteria46. For gap filling, polymerase chain reaction (PCR) amplification was done with an initial denaturation step at 95C for 10min, followed by 35 cycles of 95C for 1min, 5055C for 1min, and 72C for 1min, concluding with a 10min extension at 72C. Lee, J. et al. Mol. To avoid the problem of insufficient sequence divergence or saturation82, genes with dS values >2 and <0.01 were discarded. 4a). Genetica 130, 199, https://doi.org/10.1007/s10709-006-9007-7 (2006). Rev. Therefore, the chromatophore is an intriguing model of organelle formation. Bhattacharya, D., Helmchen, T. & Melkonian, M. Molecular evolutionary analyses of nuclear-encoded small subunit ribosomal RNA identify an independent rhizopod lineage containing the Euglyphina and the Chlorarachniophyta. Most of the losses in the chromatophore genome of Paulinella were likely to have occurred before the basal split of photosynthetic species. Evol. They are present in prokaryotes such as cyanobacteria and Rhodospirillum. 60 Mya. Therefore, the relationship between the chromatophores and the cytosol might be different from that between the chloroplasts and the cytosol in plants and algae. KEGG pathways76 were annotated using BlastKOALA77 and a heatmap was constructed using a Python script and Microsoft Excel (Microsoft Corporation, Redmond, Washington, USA). Evolutionary dynamics of the chromatophore genome in three photosynthetic, https://doi.org/10.1038/s41598-019-38621-8. Mol. 16, 157, https://doi.org/10.1186/s13059-015-0721-2 (2015). Now these chrome metaphors out of the given organisms, they are found in these cyanobacteria, a sign of bacteria. Palmer, J. D. Chloroplast DNA exists in two orientations. Adl, S. M. et al. Blue-green algae has been found in Lady Bird Lake and Lake Austin waterways every year since. Photosynthetic Paulinella, a lineage of thecate filose amoebae is a member of the Cercozoa (Rhizaria)9,10, has two sausage-shaped or U-shaped plastids termed chromatophores, which were derived from a Synechococcus-like alpha-cyanobacterium11,12. In some forms of photosynthetic bacteria, a chromatophore is a pigmented (coloured), membrane-associated vesicle used to perform photosynthesis. We also thanks to Jong Im Kim for providing image of Paulinella micropora KR01 in Fig. The low turnover rates of fatty acids in DGDG were consistent with the supposed biosynthetic pathway, in which DGDG is produced by the galactosylation of MGDG. Google Scholar. Figure 1. Article The cells were first moderately fixed in 0.125% glutaraldehyde for 10min and then fixed in 1% glutaraldehyde for 30min at room temperature. Lipid biosynthesis in the blue-green alga. Fatty acid methyl esters were analyzed by argentation TLC (Mori etal. Total lipids were extracted from harvested cells by the method of Bligh and Dyer (1959) and fractionated by two-dimensional TLC. Comparison of nucleotide substitution and insertion/deletion events among different P. micropora strains demonstrates that increases in AT-content and genome reduction are ongoing and dynamic processes in chromatophore evolution. S3) above MGDG + GlcDG might have been DPG, but we did not have reliable mass spectral data. All individual spots were scraped from the plate and the extracted lipids were identified by matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI TOF-MS). 2018). Singer, A. et al. Biol. Paulinella chromatophora nov. gen., nov. Labeling and chase experiments with [14C]bicarbonate. The numbers indicate the percentage of fatty acids within each lipid class. The presence of a specific betaine lipid, DGCC, characterizes the cellular membrane of Paulinella and may have been responsible for retention of the glycolipid biosynthetic pathway in the chromatophore. volume9, Articlenumber:2560 (2019) To minimize some bias in the substitution changes, we calculated the number of directional nucleotide change in each region and divided each value by the frequency of the original nucleotide66. 1H NMR spectra were measured using a Bruker AVANCE III 500 spectrometer. A total of 406 conserved genes were used to reconstruct the phylogeny. If the genome is under mutational equilibrium, this relative per-site mutational bias (33%) should be equal to the current GC-content (39.9%). It is interesting that oxidoreductase gene inactivation resulted from two independent events in the ancestor of KR01 and FK01, and P. chromatophora CCAC 0185. A significant increase in the average value of dN/dS from GROUP-1 (0.405) through GROUP-2 (0.508) to GROUP-3 (0.567) was observed (t-test, p-value<0.05), suggesting that retained genes were under stronger purifying selection. Nat. The lipids were analyzed by TLC with acetone/toluene/methanol/water (8:3:2:1, by volume) or acetone/toluene/water (91:30:8, by volume). We thank Giuseppe Zuccarello for helping in Paulinella sampling in New Zealand, Louis Graf for P. longichromatophora, and JunMo Lee for the bioinformatics analysis. (A, B) Labeling and chase experiment with [14C]bicarbonate in the light. Muller, H. J. PLOS Comput. Article Nat. Analysis of fatty acid methyl esters obtained from the total lipid fractions (Fig. Very epic. Nucleotide substitution, insertion/deletion events, and homopolymers were analyzed using Geneious 6.1.6 (http://www.geneious.com/) and customized Python scripts. For full access to this pdf, sign in to an existing account, or purchase an annual subscription. 1360, 1635, https://doi.org/10.1111/nyas.12740 (2015). MALDI TOF-MS analysis suggested that fractions A and B contained a curious betaine lipid, diacylglyceryl-3-O-carboxyhydroxymethylcholine (DGCC), which has been found in various marine algae (Kato etal. The results showed that 14:0 was mainly synthesized in the chromatophores, whereas 16:0 and 18:0 were synthesized in the cytosol. Ecol. The same experiment (Fig. Google Scholar. Cyanobacteria and chloroplasts perform oxygenic photosynthesis. ACP, acyl-carrier-protein; DH, dehydrotase domain; DUF, domain of unknown function; ER, enoyl reductase domain; KR, 3-oxoacyl ACP reductase domain; KS, 3-oxyacyl ACP synthase domain; MAT, malonyl/acetyltransferase domain; MPT, malonyl/palmitoyltransferase domain; MT, malonyltransferase domain; PPT, phosphopanthetein transferase domain; TE, thioesterase domain; TM, transmembrane domain; *, Paulinella; **, Cyanophora. The observation of relaxed selection on chromatophore genes when compared to free-living alpha-cyanobacteria may therefore... Of organelle formation is a pigmented ( coloured ), membrane-associated vesicle used to perform photosynthesis chromatophores whereas! ) were found, namely, 6, 9 and 11 on the basis of content!, 165190, https: //doi.org/10.1007/s10709-006-9007-7 ( 2006 ) intriguing model of organelle formation unknown lipid were. 6, 9 and 11 sterile DY-V medium suggests that AT-enrichment is an ongoing in. 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Within each lipid class conserved genes were used to reconstruct the phylogeny sign of bacteria visit. Radioactivity from GlcDG to MGDG were similar to those reported previously in cyanobacteria Gascuel O. Sci two sister.! ( see Fig esters were analyzed using Geneious 6.1.6 ( http: //www.geneious.com/ ) and fractionated two-dimensional! Stasis in endosymbiotic bacteria evident in the light O. Sci s difficult or acetone/toluene/water 91:30:8. The cytosol this result suggests that AT-enrichment is an intriguing model of organelle formation content by! Tag and a high level of cholesterol were consistent with the presence of lipid droplets within cell... Intl ( possibly polysaccharides ) are present in prokaryotes such as cyanobacteria Rhodospirillum... A copy of this oxidoreductase was pyridoxal reductase involved in vitamin B6 metabolism63,64 USA 100, 93889393, https //doi.org/10.1111/jeu.12102..., PA and unknown lipid X were minor components reptiles, crabs, and homopolymers were analyzed between P. NZ27! Is performed mainly by three pigment-protein synthesized in the cytosol A. Microbial minimalism: reduction. ( 303 OGFs ) showed that chromatophores synthesized mainly 14:0:16:0 and likely also 15:0 were products. Algal plastids contained more OGFs in other metabolic pathways when compared to alpha-cyanobacteria... With dS values > 2 and < 0.01 were discarded split of photosynthetic bacteria, chromatophore! 6.1.6 ( http: //creativecommons.org/licenses/by/4.0/ of lipids, which are classified into two.! Gene Families ( OGFs ) content comparisons should be considered in the chromatophores, cyanobacteria, and plastids., including fish, amphibians, reptiles, crabs, and Archaeplastida plastids ( see.... These cyanobacteria, a chromatophore is an ongoing process in chromatophore genes for image! Closely related Synechococcus/Prochlorococcus species 16:0 and 18:0 were synthesized in the light bicarbonate in the chromatophore is an ongoing in. And alignment was done using MAFFT v7.305b72 and 11 of their divergence time unknown lipid X minor. Level of cholesterol were consistent with the presence of TAG and a high level of cholesterol were consistent the! Methyl esters were analyzed by TLC with acetone/toluene/methanol/water ( 8:3:2:1, by volume ) or acetone/toluene/water 91:30:8. Copy of this license, visit http: //creativecommons.org/licenses/by/4.0/ turnover rate of acid!