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  • 1
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    Identification and developmental expression of the full complement of Cytochrome P450 genes in Zebrafish (2011)
    BioMed Central
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    Publication Date: 2022-05-26
    Description: © The Authors, 2010. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Genomics 11 (2010): 643, doi:10.1186/1471-2164-11-643.
    Description: Increasing use of zebrafish in drug discovery and mechanistic toxicology demands knowledge of cytochrome P450 (CYP) gene regulation and function. CYP enzymes catalyze oxidative transformation leading to activation or inactivation of many endogenous and exogenous chemicals, with consequences for normal physiology and disease processes. Many CYPs potentially have roles in developmental specification, and many chemicals that cause developmental abnormalities are substrates for CYPs. Here we identify and annotate the full suite of CYP genes in zebrafish, compare these to the human CYP gene complement, and determine the expression of CYP genes during normal development. Zebrafish have a total of 94 CYP genes, distributed among 18 gene families found also in mammals. There are 32 genes in CYP families 5 to 51, most of which are direct orthologs of human CYPs that are involved in endogenous functions including synthesis or inactivation of regulatory molecules. The high degree of sequence similarity suggests conservation of enzyme activities for these CYPs, confirmed in reports for some steroidogenic enzymes (e.g. CYP19, aromatase; CYP11A, P450scc; CYP17, steroid 17a-hydroxylase), and the CYP26 retinoic acid hydroxylases. Complexity is much greater in gene families 1, 2, and 3, which include CYPs prominent in metabolism of drugs and pollutants, as well as of endogenous substrates. There are orthologous relationships for some CYP1 s and some CYP3 s between zebrafish and human. In contrast, zebrafish have 47 CYP2 genes, compared to 16 in human, with only two (CYP2R1 and CYP2U1) recognized as orthologous based on sequence. Analysis of shared synteny identified CYP2 gene clusters evolutionarily related to mammalian CYP2 s, as well as unique clusters. Transcript profiling by microarray and quantitative PCR revealed that the majority of zebrafish CYP genes are expressed in embryos, with waves of expression of different sets of genes over the course of development. Transcripts of some CYP occur also in oocytes. The results provide a foundation for the use of zebrafish as a model in toxicological, pharmacological and chemical disease research.
    Description: This work was supported by NIH grants R01ES015912 and P42ES007381 (Superfund Basic Research Program at Boston University) (to JJS). MEJ was a Guest Investigator at the Woods Hole Oceanographic Institution (WHOI) and was supported by grants from the Swedish research council Formas and Carl Trygger's foundation. AK was a Post-doctoral Fellow at WHOI, and was supported by a fellowship from the Japanese Society for Promotion of Science (JSPS). JZ and TP were Guest Students at the WHOI and were supported by a CAPES Ph.D. Fellowship and CNPq Ph.D. Sandwich Fellowship (JZ), and by a CNPq Ph.D. Fellowship (TP), from Brazil.
    Repository Name: Woods Hole Open Access Server
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  • 2
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    Comparative transcriptome analysis of obligately asexual and cyclically sexual rotifers reveals genes with putative functions in sexual reproduction, dormancy, and asexual egg production (2013)
    BioMed Central
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    Publication Date: 2022-05-26
    Description: © The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Genomics 14 (2013): 412, doi:10.1186/1471-2164-14-412.
    Description: Sexual reproduction is a widely studied biological process because it is critically important to the genetics, evolution, and ecology of eukaryotes. Despite decades of study on this topic, no comprehensive explanation has been accepted that explains the evolutionary forces underlying its prevalence and persistence in nature. Monogonont rotifers offer a useful system for experimental studies relating to the evolution of sexual reproduction due to their rapid reproductive rate and close relationship to the putatively ancient asexual bdelloid rotifers. However, little is known about the molecular underpinnings of sex in any rotifer species. We generated mRNA-seq libraries for obligate parthenogenetic (OP) and cyclical parthenogenetic (CP) strains of the monogonont rotifer, Brachionus calyciflorus, to identify genes specific to both modes of reproduction. Our differential expression analysis identified receptors with putative roles in signaling pathways responsible for the transition from asexual to sexual reproduction. Differential expression of a specific copy of the duplicated cell cycle regulatory gene CDC20 and specific copies of histone H2A suggest that such duplications may underlie the phenotypic plasticity required for reproductive mode switch in monogononts. We further identified differential expression of genes involved in the formation of resting eggs, a process linked exclusively to sex in this species. Finally, we identified transcripts from the bdelloid rotifer Adineta ricciae that have significant sequence similarity to genes with higher expression in CP strains of B. calyciflorus. Our analysis of global gene expression differences between facultatively sexual and exclusively asexual populations of B. calyciflorus provides insights into the molecular nature of sexual reproduction in rotifers. Furthermore, our results offer insight into the evolution of obligate asexuality in bdelloid rotifers and provide indicators important for the use of monogononts as a model system for investigating the evolution of sexual reproduction.
    Description: This work was funded by National Institutes of Health Institute of General Medical Sciences (grant number 5R01GM079484, to JML and DMW).
    Keywords: Evolution of sexual reproduction ; Differential expression analysis ; Gene ontology analysis ; Meiosis ; Gametogenesis ; Resting eggs ; Mixis induction
    Repository Name: Woods Hole Open Access Server
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  • 3
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    Characterization of differential transcript abundance through time during Nematostella vectensis development (2013)
    BioMed Central
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    Publication Date: 2022-05-26
    Description: © The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Genomics 14 (2013): 266, doi:10.1186/1471-2164-14-266.
    Description: Nematostella vectensis, a burrowing sea anemone, has become a popular species for the study of cnidarian development. In previous studies, the expression of a variety of genes has been characterized during N. vectensis development with in situ mRNA hybridization. This has provided detailed spatial resolution and a qualitative perspective on changes in expression. However, little is known about broad transcriptome-level patterns of gene expression through time. Here we examine the expression of N. vectensis genes through the course of development with quantitative RNA-seq. We provide an overview of changes in the transcriptome through development, and examine the maternal to zygotic transition, which has been difficult to investigate with other tools. We measured transcript abundance in N. vectensis with RNA-seq at six time points in development: zygote (2 hours post fertilization (HPF)), early blastula (7 HPF), mid-blastula (12 HPF), gastrula (24 HPF), planula (5 days post fertilization (DPF)) and young polyp (10 DPF). The major wave of zygotic expression appears between 7–12 HPF, though some changes occur between 2–7 HPF. The most dynamic changes in transcript abundance occur between the late blastula and early gastrula stages. More transcripts are upregulated between the gastrula and planula than downregulated, and a comparatively lower number of transcripts significantly change between planula and polyp. Within the maternal to zygotic transition, we identified a subset of maternal factors that decrease early in development, and likely play a role in suppressing zygotic gene expression. Among the first genes to be expressed zygotically are genes whose proteins may be involved in the degradation of maternal RNA. The approach presented here is highly complementary to prior studies on spatial patterns of gene expression, as it provides a quantitative perspective on a broad set of genes through time but lacks spatial resolution. In addition to addressing the problems identified above, our work provides an annotated matrix that other investigators can use to examine genes and developmental events that we do not examine in detail here.
    Description: This work was supported by seed funds from the Brown-MBL Partnership and the National Science Foundation Graduate Student Research Fellowship. Infrastructure for data transfer from the sequencer was supported by the National Science Foundation EPSCoR Program under Grant No. 1004057 (Infrastructure to Advance Life Sciences in the Ocean State).
    Keywords: Nematostella vectensis ; Transcriptome ; Gene expression ; Maternal to zygotic transition ; Development
    Repository Name: Woods Hole Open Access Server
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  • 4
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    Cytochrome P450 diversity and induction by gorgonian allelochemicals in the marine gastropod Cyphoma gibbosum (2011)
    BioMed Central
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    Publication Date: 2022-05-26
    Description: © The Authors, 2010. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Ecology 10 (2010): 24, doi:10.1186/1472-6785-10-24.
    Description: Intense consumer pressure strongly affects the structural organization and function of marine ecosystems, while also having a profound effect on the phenotype of both predator and prey. Allelochemicals produced by prey often render their tissues unpalatable or toxic to a majority of potential consumers, yet some marine consumers have evolved resistance to host chemical defenses. A key challenge facing marine ecologists seeking to explain the vast differences in consumer tolerance of dietary allelochemicals is understanding the biochemical and molecular mechanisms underlying diet choice. The ability of marine consumers to tolerate toxin-laden prey may involve the cooperative action of biotransformation enzymes, including the inducible cytochrome P450s (CYPs), which have received little attention in marine invertebrates despite the importance of allelochemicals in their evolution. Here, we investigated the diversity, transcriptional response, and enzymatic activity of CYPs possibly involved in allelochemical detoxification in the generalist gastropod Cyphoma gibbosum, which feeds exclusively on chemically defended gorgonians. Twelve new genes in CYP family 4 were identified from the digestive gland of C. gibbosum. Laboratory-based feeding studies demonstrated a 2.7- to 5.1-fold induction of Cyphoma CYP4BK and CYP4BL transcripts following dietary exposure to the gorgonian Plexaura homomalla, which contains high concentrations of anti-predatory prostaglandins. Phylogenetic analysis revealed that C. gibbosum CYP4BK and CYP4BL were most closely related to vertebrate CYP4A and CYP4F, which metabolize pathophysiologically important fatty acids, including prostaglandins. Experiments involving heterologous expression of selected allelochemically-responsive C. gibbosum CYP4s indicated a possible role of one or more CYP4BL forms in eicosanoid metabolism. Sequence analysis further demonstrated that Cyphoma CYP4BK/4BL and vertebrate CYP4A/4F forms share identical amino acid residues at key positions within fatty acid substrate recognition sites. These results demonstrate differential regulation of CYP transcripts in a marine consumer feeding on an allelochemical-rich diet, and significantly advance our understanding of both the adaptive molecular mechanisms that marine consumers use to cope with environmental chemical pressures and the evolutionary history of allelochemical-metabolizing enzymes in the CYP superfamily.
    Description: Financial support for this work was provided by the Ocean Life Institute Tropical Research Initiative Grant (WHOI) to KEW and MEH; the Robert H. Cole Endowed Ocean Ventures Fund (WHOI) to KEW; the National Undersea Research Center - Program Development Proposal (CMRC-03PRMN0103A) to KEW and a National Science Foundation Graduate Research Fellowship to KEW.
    Repository Name: Woods Hole Open Access Server
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  • 5
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    Transcriptomic assessment of resistance to effects of an aryl hydrocarbon receptor (AHR) agonist in embryos of Atlantic killifish (Fundulus heteroclitus) from a marine Superfund site (2011)
    BioMed Central
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    Publication Date: 2022-05-26
    Description: © The Author(s), 2011. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Genomics 12 (2011): 263, doi:10.1186/1471-2164-12-263.
    Description: Populations of Atlantic killifish (Fundulus heteroclitus) have evolved resistance to the embryotoxic effects of polychlorinated biphenyls (PCBs) and other halogenated and nonhalogenated aromatic hydrocarbons that act through an aryl hydrocarbon receptor (AHR)-dependent signaling pathway. The resistance is accompanied by reduced sensitivity to induction of cytochrome P450 1A (CYP1A), a widely used biomarker of aromatic hydrocarbon exposure and effect, but whether the reduced sensitivity is specific to CYP1A or reflects a genome-wide reduction in responsiveness to all AHR-mediated changes in gene expression is unknown. We compared gene expression profiles and the response to 3,3',4,4',5-pentachlorobiphenyl (PCB-126) exposure in embryos (5 and 10 dpf) and larvae (15 dpf) from F. heteroclitus populations inhabiting the New Bedford Harbor, Massachusetts (NBH) Superfund site (PCB-resistant) and a reference site, Scorton Creek, Massachusetts (SC; PCB-sensitive). Analysis using a 7,000-gene cDNA array revealed striking differences in responsiveness to PCB-126 between the populations; the differences occur at all three stages examined. There was a sizeable set of PCB-responsive genes in the sensitive SC population, a much smaller set of PCB-responsive genes in NBH fish, and few similarities in PCB-responsive genes between the two populations. Most of the array results were confirmed, and additional PCB-regulated genes identified, by RNA-Seq (deep pyrosequencing). The results suggest that NBH fish possess a gene regulatory defect that is not specific to one target gene such as CYP1A but rather lies in a regulatory pathway that controls the transcriptional response of multiple genes to PCB exposure. The results are consistent with genome-wide disruption of AHR-dependent signaling in NBH fish.
    Description: This work was supported in part by National Institutes of Health grants P42ES007381 (Superfund Basic Research Program at Boston University) and by a grant from the WHOI Ocean Life Institute.
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  • 6
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    NetiNeti : discovery of scientific names from text using machine learning methods (2013)
    BioMed Central
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    Publication Date: 2022-05-26
    Description: © The Author(s), 2012. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Bioinformatics 13 (2012): 211, doi:10.1186/1471-2105-13-211.
    Description: A scientific name for an organism can be associated with almost all biological data. Name identification is an important step in many text mining tasks aiming to extract useful information from biological, biomedical and biodiversity text sources. A scientific name acts as an important metadata element to link biological information. We present NetiNeti (Name Extraction from Textual Information-Name Extraction for Taxonomic Indexing), a machine learning based approach for recognition of scientific names including the discovery of new species names from text that will also handle misspellings, OCR errors and other variations in names. The system generates candidate names using rules for scientific names and applies probabilistic machine learning methods to classify names based on structural features of candidate names and features derived from their contexts. NetiNeti can also disambiguate scientific names from other names using the contextual information. We evaluated NetiNeti on legacy biodiversity texts and biomedical literature (MEDLINE). NetiNeti performs better (precision = 98.9% and recall = 70.5%) compared to a popular dictionary based approach (precision = 97.5% and recall = 54.3%) on a 600-page biodiversity book that was manually marked by an annotator. On a small set of PubMed Central’s full text articles annotated with scientific names, the precision and recall values are 98.5% and 96.2% respectively. NetiNeti found more than 190,000 unique binomial and trinomial names in more than 1,880,000 PubMed records when used on the full MEDLINE database. NetiNeti also successfully identifies almost all of the new species names mentioned within web pages. We present NetiNeti, a machine learning based approach for identification and discovery of scientific names. The system implementing the approach can be accessed at http://namefinding.ubio.org.
    Description: This project was funded by the Ellison Medical Foundation and a grant from the National Library of Medicine (R01 LM009725).
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  • 7
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    Evidence for isolated evolution of deep-sea ciliate communities through geological separation and environmental selection (2013)
    BioMed Central
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    Publication Date: 2022-05-25
    Description: © The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Microbiology 13 (2013): 150, doi:10.1186/1471-2180-13-150.
    Description: Deep hypersaline anoxic basins (DHABs) are isolated habitats at the bottom of the eastern Mediterranean Sea, which originate from the ancient dissolution of Messinian evaporites. The different basins have recruited their original biota from the same source, but their geological evolution eventually constituted sharp environmental barriers, restricting genetic exchange between the individual basins. Therefore, DHABs are unique model systems to assess the effect of geological events and environmental conditions on the evolution and diversification of protistan plankton. Here, we examine evidence for isolated evolution of unicellular eukaryote protistan plankton communities driven by geological separation and environmental selection. We specifically focused on ciliated protists as a major component of protistan DHAB plankton by pyrosequencing the hypervariable V4 fragment of the small subunit ribosomal RNA. Geospatial distributions and responses of marine ciliates to differential hydrochemistries suggest strong physical and chemical barriers to dispersal that influence the evolution of this plankton group. Ciliate communities in the brines of four investigated DHABs are distinctively different from ciliate communities in the interfaces (haloclines) immediately above the brines. While the interface ciliate communities from different sites are relatively similar to each other, the brine ciliate communities are significantly different between sites. We found no distance-decay relationship, and canonical correspondence analyses identified oxygen and sodium as most important hydrochemical parameters explaining the partitioning of diversity between interface and brine ciliate communities. However, none of the analyzed hydrochemical parameters explained the significant differences between brine ciliate communities in different basins. Our data indicate a frequent genetic exchange in the deep-sea water above the brines. The “isolated island character” of the different brines, that resulted from geological events and contemporary environmental conditions, create selective pressures driving evolutionary processes, and with time, lead to speciation and shape protistan community composition. We conclude that community assembly in DHABs is a mixture of isolated evolution (as evidenced by small changes in V4 primary structure in some taxa) and species sorting (as indicated by the regional absence/presence of individual taxon groups on high levels in taxonomic hierarchy).
    Description: This work was funded by NSF grants OCE-0849578 and OCE- 1061774 to VE and support from Carl Zeiss fellowship to AS and from the Deutsche Forschungsgemeinschaft (grants STO414/3-2 and STO414/7-1) to TS.
    Keywords: Ciliates ; Hypersaline ; Deep-sea anoxic basins ; DHABs ; Brine ; Species sorting ; Environmental filtering ; Niche separation
    Repository Name: Woods Hole Open Access Server
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  • 8
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    The giant eyes of giant squid are indeed unexpectedly large, but not if used for spotting sperm whales (2013)
    BioMed Central
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    Publication Date: 2022-05-25
    Description: © The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Evolutionary Biology 13 (2013): 187, doi:10.1186/1471-2148-13-187.
    Description: We recently reported (Curr Biol 22:683–688, 2012) that the eyes of giant and colossal squid can grow to three times the diameter of the eyes of any other animal, including large fishes and whales. As an explanation to this extreme absolute eye size, we developed a theory for visual performance in aquatic habitats, leading to the conclusion that the huge eyes of giant and colossal squid are uniquely suited for detection of sperm whales, which are important squid-predators in the depths where these squid live. A paper in this journal by Schmitz et al. (BMC Evol Biol 13:45, 2013) refutes our conclusions on the basis of two claims: (1) using allometric data they argue that the eyes of giant and colossal squid are not unexpectedly large for the size of the squid, and (2) a revision of the values used for modelling indicates that large eyes are not better for detection of approaching sperm whales than they are for any other task. We agree with Schmitz et al. that their revised values for intensity and abundance of planktonic bioluminescence may be more realistic, or at least more appropriately conservative, but argue that their conclusions are incorrect because they have not considered some of the main arguments put forward in our paper. We also present new modelling to demonstrate that our conclusions remain robust, even with the revised input values suggested by Schmitz et al.
    Keywords: Vision ; Eyes ; Giant squid ; Sperm whale ; Bioluminescence ; Mesopelagic
    Repository Name: Woods Hole Open Access Server
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  • 9
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    Endonuclease-containing Penelope retrotransposons in the bdelloid rotifer Adineta vaga exhibit unusual structural features and play a role in expansion of host gene families (2013)
    BioMed Central
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    Publication Date: 2022-05-25
    Description: © The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Mobile DNA 4 (2013): 19, doi:10.1186/1759-8753-4-19.
    Description: Penelope-like elements (PLEs) are an enigmatic group of retroelements sharing a common ancestor with telomerase reverse transcriptases. In our previous studies, we identified endonuclease-deficient PLEs that are associated with telomeres in bdelloid rotifers, small freshwater invertebrates best known for their long-term asexuality and high foreign DNA content. Completion of the high-quality draft genome sequence of the bdelloid rotifer Adineta vaga provides us with the opportunity to examine its genomic transposable element (TE) content, as well as TE impact on genome function and evolution. We performed an exhaustive search of the A. vaga genome assembly, aimed at identification of canonical PLEs combining both the reverse transcriptase (RT) and the GIY-YIG endonuclease (EN) domains. We find that the RT/EN-containing Penelope families co-exist in the A. vaga genome with the EN-deficient RT-containing Athena retroelements. Canonical PLEs are present at very low copy numbers, often as a single-copy, and there is no evidence that they might preferentially co-mobilize EN-deficient PLEs. We also find that Penelope elements can participate in expansion of A. vaga multigene families via trans-action of their enzymatic machinery, as evidenced by identification of intron-containing host genes framed by the Penelope terminal repeats and characteristic target-site duplications generated upon insertion. In addition, we find that Penelope open reading frames (ORFs) in several families have incorporated long stretches of coding sequence several hundred amino acids (aa) in length that are highly enriched in asparagine residues, a phenomenon not observed in other retrotransposons. Our results show that, despite their low abundance and low transcriptional activity in the A. vaga genome, endonuclease-containing Penelope elements can participate in expansion of host multigene families. We conclude that the terminal repeats represent the cis-acting sequences required for mobilization of the intervening region in trans by the Penelope-encoded enzymatic activities. We also hypothesize that the unusual capture of long N-rich segments by the Penelope ORF occurs as a consequence of peculiarities of its replication mechanism. These findings emphasize the unconventional nature of Penelope retrotransposons, which, in contrast to all other retrotransposon types, are capable of dispersing intron-containing genes, thereby questioning the validity of traditional estimates of gene retrocopies in PLE-containing eukaryotic genomes.
    Description: This research was supported by grants MCB-0821956 and MCB-1121334 from the U.S. National Science Foundation to I.A.
    Keywords: Retrotransposon ; Reverse transcriptase ; GIY-YIG endonuclease
    Repository Name: Woods Hole Open Access Server
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  • 10
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    Molecular subdivision of the marine diatom Thalassiosira rotula in relation to geographic distribution, genome size, and physiology (2013)
    BioMed Central
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    Publication Date: 2022-05-25
    Description: © The Author(s), 2012. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Evolutionary Biology 12 (2012): 209, doi:10.1186/1471-2148-12-209.
    Description: Marine phytoplankton drift passively with currents, have high dispersal potentials and can be comprised of morphologically cryptic species. To examine molecular subdivision in the marine diatom Thalassiosira rotula, variations in rDNA sequence, genome size, and growth rate were examined among isolates collected from the Atlantic and Pacific Ocean basins. Analyses of rDNA included T. gravida because morphological studies have argued that T. rotula and T. gravida are conspecific. Culture collection isolates of T. gravida and T. rotula diverged by 7.0 ± 0.3% at the ITS1 and by 0.8 ± 0.03% at the 28S. Within T. rotula, field and culture collection isolates were subdivided into three lineages that diverged by 0.6 ± 0.3% at the ITS1 and 0% at the 28S. The predicted ITS1 secondary structure revealed no compensatory base pair changes among lineages. Differences in genome size were observed among isolates, but were not correlated with ITS1 lineages. Maximum acclimated growth rates of isolates revealed genotype by environment effects, but these were also not correlated with ITS1 lineages. In contrast, intra-individual variation in the multi-copy ITS1 revealed no evidence of recombination amongst lineages, and molecular clock estimates indicated that lineages diverged 0.68 Mya. The three lineages exhibited different geographic distributions and, with one exception, each field sample was dominated by a single lineage. The degree of inter- and intra-specific divergence between T. gravida and T. rotula suggests they should continue to be treated as separate species. The phylogenetic distinction of the three closely-related T. rotula lineages was unclear. On the one hand, the lineages showed no physiological differences, no consistent genome size differences and no significant changes in the ITS1 secondary structure, suggesting there are no barriers to interbreeding among lineages. In contrast, analysis of intra-individual variation in the multicopy ITS1 as well as molecular clock estimates of divergence suggest these lineages have not interbred for significant periods of time. Given the current data, these lineages should be considered a single species. Furthermore, these T. rotula lineages may be ecologically relevant, given their differential abundance over large spatial scales.
    Description: This research was supported by National Science Foundation grants, NSF 0727227 (to TAR) and NSF SBE0245039 (to URI, TAR). Part of the research was conducted using instrumentation supported by NSF-EPSCoR grants 0554548 and 1004057.
    Keywords: Phytoplankton ; Phylogeography ; Dispersal ; Physiology ; Intraspecific diversity
    Repository Name: Woods Hole Open Access Server
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