Which clades are photosynthetic

Nucleic Acids Res 30 : — Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Media for the culture of oceanic ultraphytoplankton. J Phycol 23 : — The ocean sampling day consortium. Gigascience 4 : Picocystis salinarum Chlorophyta in saline lakes and hot springs of East Africa. Phycologia 51 : 22— Pigment suites and taxonomic groups in Prasinophyceae. J Phycol 40 : — Phylogeny and molecular evolution of the green algae.

Six newly sequenced chloroplast genomes from prasinophyte green algae provide insights into the relationships among prasinophyte lineages and the diversity of streamlined genome architecture in picoplanktonic species. BMC Genomics 15 : Whole genome amplification WGA of marine photosynthetic eukaryote populations. Photosynthetic picoeukaryote community structure in the South East Pacific Ocean encompassing the most oligotrophic waters on Earth. Environ Microbiol 11 : — Picocystis salinarum gen.

Chlorophyta - a new picoplanktonic green alga. Phycologia 39 : — Li WK. Composition of ultraphytoplankton in the central north Atlantic. Mar Ecol Prog Ser : 1—8. Photosynthetic pigments of oceanic Chlorophyta belonging to prasinophytes clade VII.

J Phycol 52 : — Distribution, phylogeny, and growth of cold-adapted picoprasinophytes in Arctic seas. J Phycol 43 : 78— Swarm: robust and fast clustering method for amplicon-based studies. PeerJ 2 : e Marin B. Nested in the Chlorellales or independent class? Phylogeny and classification of the Pedinophyceae Viridiplantae revealed by molecular phylogenetic analyses of complete nuclear and plastid-encoded rRNA operons.

Marin B, Melkonian M. Molecular phylogeny and classification of the Mamiellophyceae class. Chlorophyta based on sequence comparisons of the nuclear- and plastid-encoded rRNA Operons.

Phylogenetic and ecological analysis of novel marine Stramenopiles. Appl Environ Microbiol 70 : — Distribution and abundance of uncultured heterotrophic flagellates in the world oceans.

Environ Microbiol 8 : — Phosphate transporters in marine phytoplankton and their viruses: cross-domain commonalities in viral-host gene exchanges. Environ Microbiol 14 : — Abundance and diversity of prymnesiophytes in the picoplankton community from the equatorial Pacific Ocean inferred from 18S rDNA sequences. Limnol Oceanogr 45 : 98— Gene functionalities and genome structure in Bathycoccus prasinos reflect cellular specializations at the base of the green lineage.

Genome Biol 13 : R A single species Micromonas pusilla Prasinophyceae dominates the eukaryotic picoplankton in the western English Channel. Diversity and ecology of eukaryotic marine phytoplankton. Adv Bot Res 64 : 1— J Phycol 39 : — Open science resources for the discovery and analysis of Tara Oceans data. Sci Data 2 : Convergent evolution masks extensive biodiversity among marine coccoid picoplankton. Biodivers Conserv 6 : 99— R Development Core Team.

R: a language and environment for statistical computing. R Found Stat Comput 1 : Google Scholar. Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature : — Small phytoplankton and carbon export from the surface ocean.

Science : — Diversity and productivity of photosynthetic picoeukaryotes in biogeochemically distinct regions of the South East Pacific Ocean. Limnol Oceanogr 61 : — Ecotype diversity in the marine picoeukaryote Ostreococcus Chlorophyta, Prasinophyceae. Environ Microbiol 7 : — Limnol Oceanogr 47 : — Romari K, Vaulot D. Composition and temporal variability of picoeukaryote communities at a coastal site of the English Channel from 18S rDNA sequences.

Limnol Oceanogr 49 : — Ronquist F, Huelsenbeck JP. Bioinformatics 19 : — Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev 73 : — Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75 : — PLoS One 6 : e Groups without cultured representatives dominate eukaryotic picophytoplankton in the oligotrophic South East Pacific Ocean.

Abundance and biogeography of picoprasinophyte ecotypes and other phytoplankton in the Eastern North Pacific Ocean. Appl Environ Microbiol 82 : — New insights into the nature and phylogeny of prasinophyte antenna proteins: Ostreococcus tauri , a case study. Mol Biol Evol 22 : — Influence of the Houma navigation canal on salinity patterns and landscape configuration in coastal Louisiana.

Takaichi S. Carotenoids in algae: distributions, biosyntheses and functions of carotenoids in algae. Mar Drugs 9 : — MEGA6: molecular evolutionary genetics analysis version 6. Mol Biol Evol 30 : — Diversity and ecology of green microalgae in marine systems: an overview based on 18S rRNA gene sequences. Perspect Phycol e-pub ahead of print 22 June doi Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids.

Metagenomes of the picoalga Bathycoccus from the Chile coastal upwelling. PLoS One 7 : e Wide genetic diversity of picoplanktonic green algae Chloroplastida in the Mediterranean Sea uncovered by a phylum-biased PCR approach.

Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73 : — Closely related Prochlorococcus genotypes show remarkably different depth distributions in two oceanic regions as revealed by in situ hybridization using 16S rRNA-targeted oligonucleotides.

Microbiology : — Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Assessing the dynamics and ecology of marine picophytoplankton: The importance of the eukaryotic component.

Microbial eukaryotic diversity and distribution in a river plume and cyclonic eddy-influenced ecosystem in the South China Sea. Microbiologyopen 4 : — Two decades of describing the unseen majority of aquatic microbial diversity. Mol Ecol 21 : — Download references.

We are grateful to Fabrice Not for his critical reading of the paper. You can also search for this author in PubMed Google Scholar. Correspondence to Adriana Lopes dos Santos. Reprints and Permissions. Lopes dos Santos, A. Diversity and oceanic distribution of prasinophytes clade VII, the dominant group of green algae in oceanic waters. ISME J 11, — Download citation. Regardless of which scenario is correct, these analyses both place the cyanobacterial primary endosymbiosis near the root of the eukaryotic tree, with this event occurring shortly after the split of the Plantae sensu Nozaki et al.

The primary endosymbiosis must, therefore, have occurred after the split of the Plantae from the opisthokonts and prior to the divergence of the Glaucophyta see fig.

This endosymbiotic event therefore appears to have occurred relatively soon after eukaryotic origin. Our results also show that the earliest possible date for the putative single secondary endosymbiosis in the Chromista fig. The monophyly of chromalveolate plastids Cavalier-Smith is supported by recent studies Fast et al.

The stramenopiles and haptophytes split 1, MYA fig. Each of the chromist lineages in our analyses radiated early in the Neoproterozoic e. These estimates are younger bounds because of the absence of plastid-less forms such as oomycetes and bicosoecids stramenopiles in our tree; therefore, the radiation of chromist taxa could potentially go further back into the Neoproterozoic.

We estimate the divergence of the charophyte, Chaetosphaeridium globosum Coleochaetales , to have occurred MYA node 6.

Taken together, our data suggest that the split of the glaucophytes from the red and green algae occurred early in the Mesoproterozoic, whereas the latter two groups diverged from each other in the Mesoproterozoic and radiated in the Neoproterozoic.

The estimated divergence dates using NPRS are older than those using the LF method; however, these differences are relatively minor—e. We also assessed the precision of our divergence time estimates using the credible tree set identified by Bayesian inference. This suggests that there is only minor variation in the branch length estimates in the pool of credible trees used in this analysis see fig.

We used six or five constraints in the protein analyses because node e, which was not consistent between the DNA and protein trees, had to be excluded from these calculations. Two estimates that were markedly different between the DNA- and protein-based approaches were the estimates of node a for the split of the glaucophyte 1, MYA [protein] vs.

These results reflect variation in the branch lengths that unite the glaucophyte to the cyanobacterial outgroup and to the remaining algal plastids see fig. This discordance may be resolved with increased sampling of glaucophytes or the addition of more data to the protein analysis.

Given that our divergence time estimates are reasonably accurate, then how consistent are these values with the early eukaryotic fossil record? Because the red algae are not the most anciently diverged photosynthetic eukaryotes fig. These fossil dates agree with our molecular clock estimate of about 1, MYA i. Martin et al. Our results also agree with the fossil findings of a putative eukaryotic diversification in the very late Mesoproterozoic and Neoproterozoic Knoll ; An alternative view of eukaryotic origin is provided by the Neoproterozoic snowball Earth hypothesis Cavalier-Smith ; Hoffman et al.

We wanted to address two alternative scenarios that are a consequence of the Neoproterozoic hypothesis. The first is that Bangiomorpha is not a red alga because they did not yet exist but rather an Oscillatoria -like cyanobacterium Cavalier-Smith Usage of this constraint would, therefore, lead to false, elevated age estimates for the first origin of algae. These calculations indicate that the Bangiomorpha fossil date regardless of whether the organism is a red alga or a prokaryote does not have a seriously misleading influence on our estimation procedure; rather, our clock calculations recover a date for node b that is close to this constraint 1, vs.

The second scenario we addressed is the hypothetical origin of eukaryotes MYA Cavalier-Smith ; Hoffman et al. These results suggest that forcing the snowball Earth hypothesis onto our phylogeny results in underestimates of divergence times.

Our estimate for the split of the haptophytes and stramenopiles 1, MYA fig. Their calculations supported plastid origins in haptophytes and stramenopiles at or before the Permian-Triassic boundary MYA Medlin et al.

A critical difference in our approach is that we assumed, based primarily on multi-gene phylogenetic evidence and a unique GAPDH gene duplication that is shared by chromalveolates, a monophyletic origin of chromist plastids Cavalier-Smith ; Fast et al. This implies that the common ancestor of the Chromista not just the later-diverging photosynthetic members contained the red algal secondary plastid.

Consistent with this view, a recent study has shown that the gnd gene in Phytophthora Oomycota is closely related to the homolog of cyanobacterial origin in photosynthetic stramenopiles, supporting the presence of the red algal secondary endosymbiont in Phytophthora and gnd origin through gene transfer Andersson and Roger In contrast, Medlin et al. The origin of the photosynthetic stramenopiles in their analysis would therefore represent a more recent within-group divergence and not the timing of plastid origin.

Given a photosynthetic ancestor of the haptophytes, these values bracket our date of 1, MYA for the haptophyte-stramenopile split in the plastid multi-gene tree. Assuming that our results and the Paleoproterozoic model are correct, we are left with an important problem, explaining the presence of algae significantly earlier than the eukaryotic diversification documented in Neoproterozoic fossils Anbar and Knoll We believe that this discordance likely reflects a combination of factors.

First, as mentioned above, the first appearance of a fossil is almost always an underestimate of the actual age of the lineage because of the incompleteness of the record Knoll Second, if early-diverging forms do not contain a mineralized exoskeleton e. Third, the first origin and diversification of algal groups may not have been coincident. Early red and green algae may have been unable to radiate 1, MYA because of physical factors such as nutrient conditions or tropic competition.

Anbar and Knoll suggested that low nitrogen availability which is critical for algal growth that resulted from anoxic and sulfidic oceans may have limited algal diversification in the mid-Proterozoic. Alternatively, Martin et al. In either case, these conditions were ameliorated by extensive weathering around 1, MYA, potentially laying the foundation for the Neoproterozoic algal radiation seen in the fossil record and in our molecular clock analyses fig.

Dan Graur, Associate Editor. Evolutionary relationships of algal plastids. Results of a minimum evolution ME -GTR bootstrap analysis are shown above the branches, whereas the bootstrap values from an unweighted maximum parsimony MP analysis are shown below the branches.

The bootstrap values in the gray squares were inferred from the full data set including third codon position see, figure 2 in the Supplementary Material online. The letters within the gray circles indicate nodes that were constrained for the molecular clock analyses.

The nodes that were estimated are indicated by the numbers in the filled circles. The values when all seven constraints or when the Bangiomorpha node b constraint was released are shown. Evolutionary relationships of algal plastids using the five-protein data set.

Schematic representation of the evolutionary relationships and divergence times for the red, green, glaucophyte, and chromist algae. These photosynthetic groups are outgroup-rooted with the Opisthokonta which putatively ancestrally lacked a plastid. The branches on which the cyanobacterial CB primary and red algal chromist secondary endosymbioses occurred are shown.

This work was supported by grants from the National Science Foundation awarded to D. We thank Kori Osborne for technical assistance and J. Frankel, J. Comeron, and two anonymous reviewers for critical reading of the manuscript. Anbar, A. Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science : Andersson, J.

A cyanobacterial gene in nonphotosynthetic protists—an early chloroplast acquisition in eukaryotes? Baldauf, S. The deep roots of eukaryotes. Evolutionary transfer of the chloroplast tuf A gene to the nucleus. Nature : Manhart, and J. Different fates of the chloroplast tuf A gene following its transfer to the nucleus in green algae.

USA 87 : Roger, I. Wenk-Siefert, and W. A kingdom-level phylogeny of eukaryotes based on combined protein data. Barfod, G. Albarede, A. Knoll, S. Xiao, P. Telouk, R. Frei, and J. New Lu-Hf and Pb-Pb age constraints on the earliest animal fossils. Earth Planet Sci. Benton, M. Dating the tree of life. Bhattacharya, D. The phylogeny of plastids: a review based on comparisons of small-subunit ribosomal RNA coding regions.

The actin gene of the Glaucocystophyte Cyanophora paradoxa : analysis of the coding region and introns, and an actin phylogeny of eukaryotes. Yoon, and J. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. BioEssays: 26 — Bowe, L. Coat, and C. Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales' closest relatives are conifers. USA 97 : Brasier, M. Green, A. Jephcoat, A.

Kleppe, M. Van Kranendonk, J. Lindsay, A. Steele, and N. Questioning the evidence for Earth's oldest fossils. Nature : 76 Butterfield, N. Paleobiology of the late Mesoproterozoic ca. Cavalier-Smith, T. The kingdon Chromista: origin and systematics. Round and D. Chapman, eds.

Biopress, Bristol, U. A revised six-kingdom system of life. Principles of protein and lipid targeting in secondary symbiogenesis: Euglenoid, Dinoflagellate, and Sporozoan plastid origins and the eukaryote family tree. The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification.

Crane, P. Friis, and K. The origin and early diversification of angiosperms. Nature : 27 Cutler, D. Estimating divergence times in the presence of an overdispersed molecular clock. Delsuc, F. Phillips, and D. Science Delwiche, C. The origin of plastids and their spread via secondary symbiosis. Bhattacharya, ed. Springer-Verlag, Vienna, Austria. Doyle, J. Molecules, morphology, fossils, and the relationship of angiosperms and Gnetales. Fast, N. Kissinger, D. Roos, and P. Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids.

Felsenstein, J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 : Feng, D. Cho, and R. Determining divergence times with a protein clock: update and reevaluation. USA 94 : Garcia-Ruiz, J. Hyde, A. Carnerup, A. Christy, M. Van Krankendonk, and N. Self-assembled silica-carbonate structures and detection of ancient microfossils. Gilbert, D. Transcriptome analyses of the strains grown under high light and low light revealed that the patterns of expression of the pucBA operons varied among strains grown under the same conditions.

We also found that one set of LH2 complex proteins compensated for the lack of an LH4 complex under low light intensities but not under extremely low light intensities, indicating that there is functional redundancy between some of the LH complexes under certain light intensities. The variation observed in LH gene composition and expression in Rhodopseudomonas strains likely reflects how they have evolved to adapt to light conditions in specific soil and water microenvironments.

It does this by adjusting the amount and composition of peripheral light-harvesting LH antenna complexes that it synthesizes.

Rhodopseudomonas strains are notable for containing numerous sets of light-harvesting genes.