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The red algae are an evolutionarily ancient group of predominantly marine organisms with an estimated 6000 species. Consensus higher-level molecular phylogenies support a basal split between the unicellular Cyanidiophytina and morphologically diverse Rhodophytina, the later subphylum containing most red algal species. The Rhodophytina is divided into six classes, of which five represent early diverging lineages of generally uninucleate species, whose evolutionary relationships are poorly resolved. The remaining species compose the large (27 currently recognized orders), morphologically diverse and typically multinucleate Florideophyceae. Nuclear DNA content estimates have been published for <1 % of the described red algae. The present investigation summarizes the state of our knowledge and expands our coverage of DNA content information from 196 isolates of red algae.
Numbering in excess of 10 million per milliliter of water, it is now undisputed that aquatic viruses are one of the major factors shaping the ecology and evolution of Earth's microbial world. Nonetheless, environmental viral diversity and roles remain poorly understood. Here we report the first thorough characterization of a virus (designated TsV) that infects the coastal marine microalga Tetraselmis striata. Unlike previously known microalgae-infecting viruses, TsV is a small (60 nm) DNA virus, with a 31 kb genome. From a range of eight different strains belonging to the Chlamydomonadaceae family, TsV was only able to infect T. striata. Gene expression dynamics revealed an up-regulation of viral transcripts already 1 h post-infection (p.i.). First clear signs of infection were observed 24 h p.i., with the appearance of viral factories inside the nucleus. TsV assembly was exclusively nuclear. TsV-N1 genome revealed very different from previously known algae viruses (Phycodnaviridae). Putative function and/or homology could be resolved for only 9 of the 33 ORFs encoded. Among those was a surprising DNA polymerase type Delta (only found in Eukaryotes), and two genes with closest homology to genes from human parasites of the urogenital tract. These results support the idea that the diversity of microalgae viruses goes far beyond the Phycodnaviridae family and leave the door open for future studies on implications of microalgae viruses for human health.
Symbiosis with protists is common among cnidarians such as corals and sea anemones and is associated with homeostatic and phenotypic changes in the host that could have epigenetic underpinnings, such as methylation of CpG dinucleotides. We leveraged the sensitivity to base modifications of nanopore sequencing to probe the effect of symbiosis with the chlorophyte Elliptochloris marina on methylation in the sea anemone Anthopleura elegantissima. We first validated the approach by comparison of nanopore-derived methylation levels with CpG depletion analysis of a published transcriptome, finding that high methylation levels are associated with CpG depletion as expected. Next, using reads generated exclusively from aposymbiotic anemones, a largely complete draft genome comprising 243 Mb was assembled. Reads from aposymbiotic and symbiotic sea anemones were then mapped to this genome and assessed for methylation using the program Nanopolish, which detects signal disruptions from base modifications as they pass through the nanopore. Based on assessment of 452,841 CpGs for which there was adequate read coverage (approximately 8% of the CpGs in the genome), symbiosis with E. marina was, surprisingly, associated with only subtle changes in the host methylome. However, we did identify one extended genomic region with consistently higher methylation among symbiotic individuals. The region was associated with a DNA polymerase zeta that is noted for its role in translesion synthesis, which opens interesting questions about the biology of this symbiosis. Our study highlights the power and relative simplicity of nanopore sequencing for studies of nucleic acid base modifications in non-model species.
The symbiotic relationship between cnidarians and dinoflagellates is the cornerstone of coral reef ecosystems. Although research has focused on the molecular mechanisms underlying this symbiosis, the role of epigenetic mechanisms, that is, the study of heritable changes that do not involve changes in the DNA sequence, is unknown. To assess the role of DNA methylation in the cnidarian-dinoflagellate symbiosis, we analyzed genome-wide CpG methylation, histone associations, and transcriptomic states of symbiotic and aposymbiotic anemones in the model system Aiptasia. We found that methylated genes are marked by histone 3 lysine 36 trimethylation (H3K36me3) and show significant reduction of spurious transcription and transcriptional noise, revealing a role of DNA methylation in the maintenance of transcriptional homeostasis. Changes in DNA methylation and expression show enrichment for symbiosis-related processes, such as immunity, apoptosis, phagocytosis recognition, and phagosome formation, and reveal intricate interactions between the underlying pathways. Our results demonstrate that DNA methylation provides an epigenetic mechanism of transcriptional homeostasis that responds to symbiosis.
Sampling expeditions to Churchill in the Canadian subarctic were completed with the aim of compiling a molecular-assisted survey of the macroalgal flora (seaweeds) for comparison to published accounts for this area, which are based on morphological identifications. Further, because the Churchill region was covered by ice until recently (~10,000 before present), the current algal flora has had to migrate from adjacent waters into that region. We used our DNA barcode data to predict the relative contribution of the North Atlantic and North Pacific floras (Likely Source Region) in repopulating the Churchill region following the most recent glacial retreat.
C5-glyceryl-methylcytosine (5gmC) is a novel DNA modification catalyzed by algal TET homologue CMD1 using vitamin C (VC) as co-substrate. Here, we report the structures of CMD1 in apo form and in complexes with VC or/and dsDNA. CMD1 exhibits comparable binding affinities for DNAs of different lengths, structures, and 5mC levels, and displays a moderate substrate preference for 5mCpG-containing DNA. CMD1 adopts the typical DSBH fold of Fe2+/2-OG-dependent dioxygenases. The lactone form of VC binds to the active site and mono-coordinates the Fe2+ in a manner different from 2-OG. The dsDNA binds to a positively charged cleft of CMD1 and the 5mC/C is inserted into the active site and recognized by CMD1 in a similar manner as the TET proteins. The functions of key residues are validated by mutagenesis and activity assay. Our structural and biochemical data together reveal the molecular mechanism for the VC-derived 5gmC DNA modification by CMD1.
Algae are smaller organisms than land plants and offer clear advantages in research over terrestrial species in terms of rapid production, short generation time and varied commercial applications. Thus, studies investigating the practical development of effective algal production are important and will improve our understanding of both aquatic and terrestrial plants. In this study we estimated multiple physicochemical and secondary structural properties of protein sequences, the predicted presence of post-translational modification (PTM) sites, and subcellular localization using a total of 510,123 protein sequences from the proteomes of 31 algal and three plant species. Algal species were broadly selected from green and red algae, glaucophytes, oomycetes, diatoms and other microalgal groups. The results were deposited in the Algal Protein Annotation Suite database (Alga-PrAS; http://alga-pras.riken.jp/), which can be freely accessed online.
To clarify the establishment process of coral-algal symbiotic relationships, coral transcriptome changes during increasing algal symbiont densities were examined in juvenile corals following inoculation with the algae Symbiodinium goreaui (clade C) and S. trenchii (clade D), and comparison of their transcriptomes with aposymbiotic corals by RNA-sequencing. Since Symbiodinium clades C and D showed very different rates of density increase, comparisons were made of early onsets of both symbionts, revealing that the host behaved differently for each. RNA-sequencing showed that the number of differentially-expressed genes in corals colonized by clade D increased ca. two-fold from 10 to 20 days, whereas corals with clade C showed unremarkable changes consistent with a slow rate of density increase. The data revealed dynamic metabolic changes in symbiotic corals. In addition, the endocytosis pathway was also upregulated, while lysosomal digestive enzymes and the immune system tended to be downregulated as the density of clade D algae increased. The present dataset provides an enormous number of candidate symbiosis-related molecules that exhibit the detailed process by which coral-algal endosymbiosis is established.
Coralline algae form extensive maerl and rhodolith habitats that support a rich biodiversity. Calcium carbonate harvesting as well as trawling activities threatens this ecosystem. Eleven species were recorded so far as maerl-forming in NE Atlantic, but identification based on morphological characters is unreliable. As for most red algae, we now use molecular characters to resolve identification of these taxa. However, obtaining DNA sequences requires time and resource demanding methods. The purpose of our study was to improve methods for achieving simple DNA extraction, amplification, sequencing and sequence analysis to allow robust identification of maerl species and other coralline algae. Our novel and easy DNA preparation method for coralline algae was of sufficient quality for qPCR amplification and sequencing of all 47 tested samples. The new psbA qPCR assay successfully amplified a 350 bp fragment identifying six species and uncovering two new Operational Taxonomic Units. Molecular results were corroborated with anatomical examination using i.e. scanning electron microscopy. Finally, the qPCR assay was coupled with High Resolution Melt analysis that successfully differentiated the closely related species Lithothamnion erinaceum and L. cf. glaciale. This DNA preparation and qPCR technique should vitalize coralline research by reducing time and cost associated with molecular systematics.
Megaviruses are generically defined as giant viruses with genomes up to 1.26Mb that infect eukaryotic unicellular protists; they are clearly delineated in DNA polymerase B phylogenetic trees; in addition, common features often include an associated virophage observed during infection; the presence of an amino acyl tRNA synthetase gene; and a nucleic acid mismatch repair protein, MutS gene. The archetypal representative of this evolving putative family is Mimivirus, an opportunistic pathogen of Acanthamoeba spp. originally thought to be a bacterium until its genome sequence was published in 2004. Subsequent analysis of marine metagenomic data revealed Megaviruses are likely ubiquitous on the surface ocean. Analysis of genome sequences of giant viruses isolated from naturally occurring marine protists such as microalgae and a microflagellate grazer, started the expansion of the Megaviridae. Here, we explored the possibility of developing Megavirus specific markers for mutS that could be used in virus molecular ecology studies. MutS is split into 15 different clades representing a wide range of cellular life, and two that contain Megaviruses, clade MutS7 and clade MutS8. We developed specific PCR primers that recognized Megavirus clade MutS8, a clade that we propose discriminates most of the algal Megaviruses. Analysis of seawater off the coast of Maine, US, revealed novel groups of algal Megaviruses that were present in all samples tested. The Megavirus clade MutS8 marker should be considered as a tool to reveal new diversity and distribution of this enigmatic group of viruses.
Mutualistic interactions between free-living algae and fungi are widespread in nature and are hypothesized to have facilitated the evolution of land plants and lichens. In all known algal-fungal mutualisms, including lichens, algal cells remain external to fungal cells. Here, we report on an algal-fungal interaction in which Nannochloropsis oceanica algal cells become internalized within the hyphae of the fungus Mortierella elongata. This apparent symbiosis begins with close physical contact and nutrient exchange, including carbon and nitrogen transfer between fungal and algal cells as demonstrated by isotope tracer experiments. This mutualism appears to be stable, as both partners remain physiologically active over months of co-cultivation, leading to the eventual internalization of photosynthetic algal cells, which persist to function, grow and divide within fungal hyphae. Nannochloropsis and Mortierella are biotechnologically important species for lipids and biofuel production, with available genomes and molecular tool kits. Based on the current observations, they provide unique opportunities for studying fungal-algal mutualisms including mechanisms leading to endosymbiosis.
The Plantae comprising red, green (including land plants), and glaucophyte algae are postulated to have a single common ancestor that is the founding lineage of photosynthetic eukaryotes. However, recent multiprotein phylogenies provide little or no support for this hypothesis. This may reflect limited complete genome data available for red algae, currently only the highly reduced genome of Cyanidioschyzon merolae, a reticulate gene ancestry, or variable gene divergence rates that mislead phylogenetic inference. Here, using novel genome data from the mesophilic Porphyridium cruentum and Calliarthron tuberculosum, we analyze 60,000 novel red algal genes to test the monophyly of red + green (RG) algae and their extent of gene sharing with other lineages. Using a gene-by-gene approach, we find an emerging signal of RG monophyly (supported by ∼50% of the examined protein phylogenies) that increases with the number of distinct phyla and terminal taxa in the analysis. A total of 1,808 phylogenies show evidence of gene sharing between Plantae and other lineages. We demonstrate that a rich mesophilic red algal gene repertoire is crucial for testing controversial issues in eukaryote evolution and for understanding the complex patterns of gene inheritance in protists.
Photosystem I (PSI) with its associated light-harvesting system is the most important generator of reducing power in photosynthesis. The PSI core complex is highly conserved, whereas peripheral subunits as well as light-harvesting proteins (LHCI) reveal a dynamic plasticity. Moreover, in green alga, PSI-LHCI complexes are found as monomers, dimers, and state transition complexes, where two LHCII trimers are associated. Herein, we show light-dependent phosphorylation of PSI subunits PsaG and PsaH as well as Lhca6. Potential consequences of the dynamic phosphorylation of PsaG and PsaH are structurally analyzed and discussed in regard to the formation of the monomeric, dimeric, and LHCII-associated PSI-LHCI complexes.
Acanthamoeba polyphaga mimivirus is the largest known ds-DNA virus and its 1.2 Mb-genome sequence has revealed many unique features. Mimivirus occupies an independent lineage among eukaryotic viruses and its known hosts include only species from the Acanthamoeba genus. The existence of mimivirus relatives was first suggested by the analysis of the Sargasso Sea metagenomic data.
The formation of sinking particles in the ocean, which promote carbon sequestration into deeper water and sediments, involves algal polysaccharides acting as an adhesive, binding together molecules, cells and minerals. These as yet unidentified adhesive polysaccharides must resist degradation by bacterial enzymes or else they dissolve and particles disassemble before exporting carbon. Here, using monoclonal antibodies as analytical tools, we trace the abundance of 27 polysaccharide epitopes in dissolved and particulate organic matter during a series of diatom blooms in the North Sea, and discover a fucose-containing sulphated polysaccharide (FCSP) that resists enzymatic degradation, accumulates and aggregates. Previously only known as a macroalgal polysaccharide, we find FCSP to be secreted by several globally abundant diatom species including the genera Chaetoceros and Thalassiosira. These findings provide evidence for a novel polysaccharide candidate to contribute to carbon sequestration in the ocean.
Several theories for aging are constantly put forth to explain the underlying mechanisms. Oxidative stress, DNA dysfunction, inflammation, and mitochondrial dysfunction, along with the release of cytochrome c are some of these theories. Diseases such as type 2 diabetes mellitus, intestinal dysfunction, cardiovascular diseases, hepatic injury, and even cancer develop with age and eventually cause death. Ulva polysaccharides, owing to their special structures and various functions, have emerged as desirable materials for keeping healthy. These polysaccharide structures are found to be closely related to the extraction methods, seaweed strains, and culture conditions. Ulvan is a promising bioactive substance, a potential functional food, which can regulate immune cells to augment inflammation, control the activity of aging-related genes, promote tumor senescence, enhance mitochondrial function, maintain liver balance, and protect the gut microbiome from inflammatory attacks. Given the desirable physiochemical and gelling properties of ulvan, it would serve to improve the quality and shelf-life of food.
Unicellular algae, termed phytoplankton, greatly impact the marine environment by serving as the basis of marine food webs and by playing central roles in the biogeochemical cycling of elements. The interactions between phytoplankton and heterotrophic bacteria affect the fitness of both partners. It is becoming increasingly recognized that metabolic exchange determines the nature of such interactions, but the underlying molecular mechanisms remain underexplored. Here, we investigated the molecular and metabolic basis for the bacterial lifestyle switch, from coexistence to pathogenicity, in Sulfitobacter D7 during its interaction with Emiliania huxleyi, a cosmopolitan bloom-forming phytoplankter. To unravel the bacterial lifestyle switch, we analyzed bacterial transcriptomes in response to exudates derived from algae in exponential growth and stationary phase, which supported the Sulfitobacter D7 coexistence and pathogenicity lifestyles, respectively. In pathogenic mode, Sulfitobacter D7 upregulated flagellar motility and diverse transport systems, presumably to maximize assimilation of E. huxleyi-derived metabolites released by algal cells upon cell death. Algal dimethylsulfoniopropionate (DMSP) was a pivotal signaling molecule that mediated the transition between the lifestyles, supporting our previous findings. However, the coexisting and pathogenic lifestyles were evident only in the presence of additional algal metabolites. Specifically, we discovered that algae-produced benzoate promoted the growth of Sulfitobacter D7 and hindered the DMSP-induced lifestyle switch to pathogenicity, demonstrating that benzoate is important for maintaining the coexistence of algae and bacteria. We propose that bacteria can sense the physiological state of the algal host through changes in the metabolic composition, which will determine the bacterial lifestyle during interaction.
Diatoms, considered as one of the most diverse and largest groups of algae, can provide the means to reach a sustainable production of petrochemical substitutes and bioactive compounds. However, a prerequisite to achieving this goal is to increase the solar-to-biomass conversion efficiency of photosynthesis, which generally remains less than 5% for most photosynthetic organisms. We have developed and implemented a rapid and effective approach, herein referred to as intracellular spectral recompositioning (ISR) of light, which, through absorption of excess blue light and its intracellular emission in the green spectral band, can improve light utilization. We demonstrate that ISR can be used chemogenically, by using lipophilic fluorophores, or biogenically, through the expression of an enhanced green fluorescent protein (eGFP) in the model diatom Phaeodactylum tricornutum. Engineered P. tricornutum cells expressing eGFP achieved 28% higher efficiency in photosynthesis than the parental strain, along with an increased effective quantum yield and reduced nonphotochemical quenching (NPQ) induction levels under high-light conditions. Further, pond simulator experiments demonstrated that eGFP transformants could outperform their wild-type parental strain by 50% in biomass production rate under simulated outdoor sunlight conditions. Transcriptome analysis identified up-regulation of major photosynthesis genes in the engineered strain in comparison with the wild type, along with down-regulation of NPQ genes involved in light stress response. Our findings provide a proof of concept for a strategy of developing more efficient photosynthetic cell factories to produce algae-based biofuels and bioactive products.
Organellar genomes serve as useful models for genome evolution and contain some of the most widely used phylogenetic markers, but they are poorly characterized in many lineages. Here, we report 20 novel mitochondrial genomes and 16 novel plastid genomes from the brown algae. We focused our efforts on the orders Chordales and Laminariales but also provide the first plastid genomes (plastomes) from Desmarestiales and Sphacelariales, the first mitochondrial genome (mitome) from Ralfsiales and a nearly complete mitome from Sphacelariales. We then compared gene content, sequence evolution rates, shifts in genome structural arrangements, and intron distributions across lineages. We confirm that gene content is largely conserved in both organellar genomes across the brown algal tree of life, with few cases of gene gain or loss. We further show that substitution rates are generally lower in plastid than mitochondrial genes, but plastomes are more variable in gene arrangement, as mitomes tend to be colinear even among distantly related lineages (with exceptions). Patterns of intron distribution across organellar genomes are complex. In particular, the mitomes of several laminarialean species possess group II introns that have T7-like ORFs, found previously only in mitochondrial genomes of Pylaiella spp. (Ectocarpales). The distribution of these mitochondrial introns is inconsistent with vertical transmission and likely reflects invasion by horizontal gene transfer between lineages. In the most extreme case, the mitome of Hedophyllum nigripes is ∼40% larger than the mitomes of close relatives because of these introns. Our results provide substantial insight into organellar evolution across the brown algae.
Planctomycetes are bacteria with complex molecular and cellular biology. They have large genomes, some over 7Mb, and complex life cycles that include motile cells and sessile cells. Some live on the complex biofilm of macroalgae. Factors governing their life in this environment were investigated at the genomic level. We analyzed the genomes of three planctomycetes isolated from algal surfaces. The genomes were 6.6Mbp to 8.1Mbp large. Genes for outer-membrane proteins, peptidoglycan and lipopolysaccharide biosynthesis were present. Rubripirellula obstinata LF1T, Roseimaritima ulvae UC8T and Mariniblastus fucicola FC18T shared with Rhodopirellula baltica and R. rubra SWK7 unique proteins related to metal binding systems, phosphate metabolism, chemotaxis, and stress response. These functions may contribute to their ecological success in such a complex environment. Exceptionally huge proteins (6000 to 10,000 amino-acids) with extracellular, periplasmic or membrane-associated locations were found which may be involved in biofilm formation or cell adhesion.
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