Publications by authors named "John McCrow"

28 Publications

  • Page 1 of 1

Dinoflagellates alter their carbon and nutrient metabolic strategies across environmental gradients in the central Pacific Ocean.

Nat Microbiol 2021 02 4;6(2):173-186. Epub 2021 Jan 4.

Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA.

Marine microeukaryotes play a fundamental role in biogeochemical cycling through the transfer of energy to higher trophic levels and vertical carbon transport. Despite their global importance, microeukaryote physiology, nutrient metabolism and contributions to carbon cycling across offshore ecosystems are poorly characterized. Here, we observed the prevalence of dinoflagellates along a 4,600-km meridional transect extending across the central Pacific Ocean, where oligotrophic gyres meet equatorial upwelling waters rich in macronutrients yet low in dissolved iron. A combined multi-omics and geochemical analysis provided a window into dinoflagellate metabolism across the transect, indicating a continuous taxonomic dinoflagellate community that shifted its functional transcriptome and proteome as it extended from the euphotic to the mesopelagic zone. In euphotic waters, multi-omics data suggested that a combination of trophic modes were utilized, while mesopelagic metabolism was marked by cytoskeletal investments and nutrient recycling. Rearrangement in nutrient metabolism was evident in response to variable nitrogen and iron regimes across the gradient, with no associated change in community assemblage. Total dinoflagellate proteins scaled with particulate carbon export, with both elevated in equatorial waters, suggesting a link between dinoflagellate abundance and total carbon flux. Dinoflagellates employ numerous metabolic strategies that enable broad occupation of central Pacific ecosystems and play a dual role in carbon transformation through both photosynthetic fixation in the euphotic zone and remineralization in the mesopelagic zone.
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http://dx.doi.org/10.1038/s41564-020-00814-7DOI Listing
February 2021

Sierra Nevada mountain lake microbial communities are structured by temperature, resources and geographic location.

Mol Ecol 2020 06 24;29(11):2080-2093. Epub 2020 Jun 24.

Division of Biological Sciences, University of California San Diego, La Jolla, CA, USA.

Warming, eutrophication (nutrient fertilization) and brownification (increased loading of allochthonous organic matter) are three global trends impacting lake ecosystems. However, the independent and synergistic effects of resource addition and warming on autotrophic and heterotrophic microorganisms are largely unknown. In this study, we investigate the independent and interactive effects of temperature, dissolved organic carbon (DOC, both allochthonous and autochthonous) and nitrogen (N) supply, in addition to the effect of spatial variables, on the composition, richness, and evenness of prokaryotic and eukaryotic microbial communities in lakes across elevation and N deposition gradients in the Sierra Nevada mountains of California, USA. We found that both prokaryotic and eukaryotic communities are structured by temperature, terrestrial (allochthonous) DOC and latitude. Prokaryotic communities are also influenced by total and aquatic (autochthonous) DOC, while eukaryotic communities are also structured by nitrate. Additionally, increasing N availability was associated with reduced richness of prokaryotic communities, and both lower richness and evenness of eukaryotes. We did not detect any synergistic or antagonistic effects as there were no interactions among temperature and resource variables. Together, our results suggest that (a) organic and inorganic resources, temperature, and geographic location (based on latitude and longitude) independently influence lake microbial communities; and (b) increasing N supply due to atmospheric N deposition may reduce richness of both prokaryotic and eukaryotic microbes, probably by reducing niche dimensionality. Our study provides insight into abiotic processes structuring microbial communities across environmental gradients and their potential roles in material and energy fluxes within and between ecosystems.
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http://dx.doi.org/10.1111/mec.15469DOI Listing
June 2020

Evolution and regulation of nitrogen flux through compartmentalized metabolic networks in a marine diatom.

Nat Commun 2019 10 7;10(1):4552. Epub 2019 Oct 7.

Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, 92037, USA.

Diatoms outcompete other phytoplankton for nitrate, yet little is known about the mechanisms underpinning this ability. Genomes and genome-enabled studies have shown that diatoms possess unique features of nitrogen metabolism however, the implications for nutrient utilization and growth are poorly understood. Using a combination of transcriptomics, proteomics, metabolomics, fluxomics, and flux balance analysis to examine short-term shifts in nitrogen utilization in the model pennate diatom in Phaeodactylum tricornutum, we obtained a systems-level understanding of assimilation and intracellular distribution of nitrogen. Chloroplasts and mitochondria are energetically integrated at the critical intersection of carbon and nitrogen metabolism in diatoms. Pathways involved in this integration are organelle-localized GS-GOGAT cycles, aspartate and alanine systems for amino moiety exchange, and a split-organelle arginine biosynthesis pathway that clarifies the role of the diatom urea cycle. This unique configuration allows diatoms to efficiently adjust to changing nitrogen status, conferring an ecological advantage over other phytoplankton taxa.
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http://dx.doi.org/10.1038/s41467-019-12407-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6779911PMC
October 2019

Silicon limitation facilitates virus infection and mortality of marine diatoms.

Nat Microbiol 2019 11 15;4(11):1790-1797. Epub 2019 Jul 15.

Department of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ, USA.

Diatoms are among the most globally distributed and ecologically successful organisms in the modern ocean, contributing upwards of 40% of total marine primary productivity. By converting dissolved silicon into biogenic silica, and photosynthetically fixing carbon dioxide into particulate organic carbon, diatoms effectively couple the silicon (Si) and carbon cycles and ballast substantial vertical flux of carbon out of the euphotic zone into the mesopelagic and deep ocean. Viruses are key players in ocean biogeochemical cycles, yet little is known about how viral infection specifically impacts diatom populations. Here, we show that Si limitation facilitates virus infection and mortality in diatoms in the highly productive coastal waters of the California Current Ecosystem. Using metatranscriptomic analysis of cell-associated diatom viruses and targeted quantification of extracellular viruses, we found a link between Si stress and the early, active and lytic stages of viral infection. This relationship was also observed in cultures of the bloom-forming diatom Chaetoceros tenuissimus, where Si stress accelerated virus-induced mortality. Together, these findings contextualize viruses within the ecophysiological framework of Si availability and diatom-mediated biogeochemical cycling.
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http://dx.doi.org/10.1038/s41564-019-0502-xDOI Listing
November 2019

Biosynthesis of the neurotoxin domoic acid in a bloom-forming diatom.

Science 2018 09;361(6409):1356-1358

Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093, USA.

Oceanic harmful algal blooms of diatoms produce the potent mammalian neurotoxin domoic acid (DA). Despite decades of research, the molecular basis for its biosynthesis is not known. By using growth conditions known to induce DA production in , we implemented transcriptome sequencing in order to identify DA biosynthesis genes that colocalize in a genomic four-gene cluster. We biochemically investigated the recombinant DA biosynthetic enzymes and linked their mechanisms to the construction of DA's diagnostic pyrrolidine skeleton, establishing a model for DA biosynthesis. Knowledge of the genetic basis for toxin production provides an orthogonal approach to bloom monitoring and enables study of environmental factors that drive oceanic DA production.
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http://dx.doi.org/10.1126/science.aau0382DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6276376PMC
September 2018

Tracking the rise of eukaryotes to ecological dominance with zinc isotopes.

Geobiology 2018 07 5;16(4):341-352. Epub 2018 Jun 5.

Geology and Geophysics, Yale University, New Haven, Connecticut.

The biogeochemical cycling of zinc (Zn) is intimately coupled with organic carbon in the ocean. Based on an extensive new sedimentary Zn isotope record across Earth's history, we provide evidence for a fundamental shift in the marine Zn cycle ~800 million years ago. We discuss a wide range of potential drivers for this transition and propose that, within available constraints, a restructuring of marine ecosystems is the most parsimonious explanation for this shift. Using a global isotope mass balance approach, we show that a change in the organic Zn/C ratio is required to account for observed Zn isotope trends through time. Given the higher affinity of eukaryotes for Zn relative to prokaryotes, we suggest that a shift toward a more eukaryote-rich ecosystem could have provided a means of more efficiently sequestering organic-derived Zn. Despite the much earlier appearance of eukaryotes in the microfossil record (~1700 to 1600 million years ago), our data suggest a delayed rise to ecological prominence during the Neoproterozoic, consistent with the currently accepted organic biomarker records.
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http://dx.doi.org/10.1111/gbi.12289DOI Listing
July 2018

Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms.

Nature 2018 03 14;555(7697):534-537. Epub 2018 Mar 14.

J. Craig Venter Institute, Microbial and Environmental Genomics, La Jolla, California 92037, USA.

In vast areas of the ocean, the scarcity of iron controls the growth and productivity of phytoplankton. Although most dissolved iron in the marine environment is complexed with organic molecules, picomolar amounts of labile inorganic iron species (labile iron) are maintained within the euphotic zone and serve as an important source of iron for eukaryotic phytoplankton and particularly for diatoms. Genome-enabled studies of labile iron utilization by diatoms have previously revealed novel iron-responsive transcripts, including the ferric iron-concentrating protein ISIP2A, but the mechanism behind the acquisition of picomolar labile iron remains unknown. Here we show that ISIP2A is a phytotransferrin that independently and convergently evolved carbonate ion-coordinated ferric iron binding. Deletion of ISIP2A disrupts high-affinity iron uptake in the diatom Phaeodactylum tricornutum, and uptake is restored by complementation with human transferrin. ISIP2A is internalized by endocytosis, and manipulation of the seawater carbonic acid system reveals a second-order dependence on the concentrations of labile iron and carbonate ions. In P. tricornutum, the synergistic interaction of labile iron and carbonate ions occurs at environmentally relevant concentrations, revealing that carbonate availability co-limits iron uptake. Phytotransferrin sequences have a broad taxonomic distribution and are abundant in marine environmental genomic datasets, suggesting that acidification-driven declines in the concentration of seawater carbonate ions will have a negative effect on this globally important eukaryotic iron acquisition mechanism.
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http://dx.doi.org/10.1038/nature25982DOI Listing
March 2018

Contrasting effects of copper limitation on the photosynthetic apparatus in two strains of the open ocean diatom Thalassiosira oceanica.

PLoS One 2017 24;12(8):e0181753. Epub 2017 Aug 24.

Department of Earth, Ocean, and Atmospheric Sciences, University of British Columbia, Vancouver, British Columbia, Canada.

There is an intricate interaction between iron (Fe) and copper (Cu) physiology in diatoms. However, strategies to cope with low Cu are largely unknown. This study unveils the comprehensive restructuring of the photosynthetic apparatus in the diatom Thalassiosira oceanica (CCMP1003) in response to low Cu, at the physiological and proteomic level. The restructuring results in a shift from light harvesting for photochemistry-and ultimately for carbon fixation-to photoprotection, reducing carbon fixation and oxygen evolution. The observed decreases in the physiological parameters Fv/Fm, carbon fixation, and oxygen evolution, concomitant with increases in the antennae absorption cross section (σPSII), non-photochemical quenching (NPQ) and the conversion factor (φe:C/ηPSII) are in agreement with well documented cellular responses to low Fe. However, the underlying proteomic changes due to low Cu are very different from those elicited by low Fe. Low Cu induces a significant four-fold reduction in the Cu-containing photosynthetic electron carrier plastocyanin. The decrease in plastocyanin causes a bottleneck within the photosynthetic electron transport chain (ETC), ultimately leading to substantial stoichiometric changes. Namely, 2-fold reduction in both cytochrome b6f complex (cytb6f) and photosystem II (PSII), no change in the Fe-rich PSI and a 40- and 2-fold increase in proteins potentially involved in detoxification of reactive oxygen species (ferredoxin and ferredoxin:NADP+ reductase, respectively). Furthermore, we identify 48 light harvesting complex (LHC) proteins in the publicly available genome of T. oceanica and provide proteomic evidence for 33 of these. The change in the LHC composition within the antennae in response to low Cu underlines the shift from photochemistry to photoprotection in T. oceanica (CCMP1003). Interestingly, we also reveal very significant intra-specific strain differences. Another strain of T. oceanica (CCMP 1005) requires significantly higher Cu concentrations to sustain both its maximal and minimal growth rate compared to CCMP 1003. Under low Cu, CCMP 1005 decreases its growth rate, cell size, Chla and total protein per cell. We argue that the reduction in protein per cell is the main strategy to decrease its cellular Cu requirement, as none of the other parameters tested are affected. Differences between the two strains, as well as differences between the well documented responses to low Fe and those presented here in response to low Cu are discussed.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0181753PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5570362PMC
October 2017

Nitrate Reductase Knockout Uncouples Nitrate Transport from Nitrate Assimilation and Drives Repartitioning of Carbon Flux in a Model Pennate Diatom.

Plant Cell 2017 Aug 1;29(8):2047-2070. Epub 2017 Aug 1.

Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, California 92037

The ecological prominence of diatoms in the ocean environment largely results from their superior competitive ability for dissolved nitrate (NO). To investigate the cellular and genetic basis of diatom NO assimilation, we generated a knockout in the nitrate reductase gene (-KO) of the model pennate diatom In -KO cells, N-assimilation was abolished although NO transport remained intact. Unassimilated NO accumulated in -KO cells, resulting in swelling and associated changes in biochemical composition and physiology. Elevated expression of genes encoding putative vacuolar NO chloride channel transporters plus electron micrographs indicating enlarged vacuoles suggested vacuolar storage of NO Triacylglycerol concentrations in the -KO cells increased immediately following the addition of NO, and these increases coincided with elevated gene expression of key triacylglycerol biosynthesis components. Simultaneously, induction of transcripts encoding proteins involved in thylakoid membrane lipid recycling suggested more abrupt repartitioning of carbon resources in -KO cells compared with the wild type. Conversely, ribosomal structure and photosystem genes were immediately deactivated in -KO cells following NO addition, followed within hours by deactivation of genes encoding enzymes for chlorophyll biosynthesis and carbon fixation and metabolism. N-assimilation pathway genes respond uniquely, apparently induced simultaneously by both NO replete and deplete conditions.
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http://dx.doi.org/10.1105/tpc.16.00910DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5590495PMC
August 2017

The Baltic Sea Virome: Diversity and Transcriptional Activity of DNA and RNA Viruses.

mSystems 2017 Jan-Feb;2(1). Epub 2017 Feb 14.

Microbial and Environmental Genomics, J. Craig Venter Institute, San Diego, California, USA.

Metagenomic and metatranscriptomic data were generated from size-fractionated samples from 11 sites within the Baltic Sea and adjacent marine waters of Kattegat and freshwater Lake Torneträsk in order to investigate the diversity, distribution, and transcriptional activity of virioplankton. Such a transect, spanning a salinity gradient from freshwater to the open sea, facilitated a broad genome-enabled investigation of natural as well as impacted aspects of Baltic Sea viral communities. Taxonomic signatures representative of phages within the widely distributed order were identified with enrichments in lesser-known families such as and . The distribution of phage reported to infect diverse and ubiquitous heterotrophic bacteria (SAR11 clades) and cyanobacteria ( sp.) displayed population-level shifts in diversity. Samples from higher-salinity conditions (>14 practical salinity units [PSU]) had increased abundances of viruses for picoeukaryotes, i.e., . These data, combined with host diversity estimates, suggest viral modulation of diversity on the whole-community scale, as well as in specific prokaryotic and eukaryotic lineages. RNA libraries revealed single-stranded DNA (ssDNA) and RNA viral populations throughout the Baltic Sea, with ssDNA phage highly represented in Lake Torneträsk. Further, our data suggest relatively high transcriptional activity of fish viruses within diverse families known to have broad host ranges, such as (RNA), (DNA), and predicted zoonotic viruses that can cause ecological and economic damage as well as impact human health. Inferred virus-host relationships, community structures of ubiquitous ecologically relevant groups, and identification of transcriptionally active populations have been achieved with our Baltic Sea study. Further, these data, highlighting the transcriptional activity of viruses, represent one of the more powerful uses of omics concerning ecosystem health. The use of omics-related data to assess ecosystem health holds great promise for rapid and relatively inexpensive determination of perturbations and risk, explicitly with regard to viral assemblages, as no single marker gene is suitable for widespread taxonomic coverage.
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http://dx.doi.org/10.1128/mSystems.00125-16DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5309335PMC
February 2017

Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation.

PLoS Genet 2016 Dec 14;12(12):e1006490. Epub 2016 Dec 14.

Integrative Oceanography Division, Scripps Institution of Oceanography, UC San Diego, La Jolla, California, United States of America.

Environmental fluctuations affect distribution, growth and abundance of diatoms in nature, with iron (Fe) availability playing a central role. Studies on the response of diatoms to low Fe have either utilized continuous (24 hr) illumination or sampled a single time of day, missing any temporal dynamics. We profiled the physiology, metabolite composition, and global transcripts of the pennate diatom Phaeodactylum tricornutum during steady-state growth at low, intermediate, and high levels of dissolved Fe over light:dark cycles, to better understand fundamental aspects of genetic control of physiological acclimation to growth under Fe-limitation. We greatly expand the catalog of genes involved in the low Fe response, highlighting the importance of intracellular trafficking in Fe-limited diatoms. P. tricornutum exhibited transcriptomic hallmarks of slowed growth leading to prolonged periods of cell division/silica deposition, which could impact biogeochemical carbon sequestration in Fe-limited regions. Light harvesting and ribosome biogenesis transcripts were generally reduced under low Fe while transcript levels for genes putatively involved in the acquisition and recycling of Fe were increased. We also noted shifts in expression towards increased synthesis and catabolism of branched chain amino acids in P. tricornutum grown at low Fe whereas expression of genes involved in central core metabolism were relatively unaffected, indicating that essential cellular function is protected. Beyond the response of P. tricornutum to low Fe, we observed major coordinated shifts in transcript control of primary and intermediate metabolism over light:dark cycles which contribute to a new view of the significance of distinctive diatom pathways, such as mitochondrial glycolysis and the ornithine-urea cycle. This study provides new insight into transcriptional modulation of diatom physiology and metabolism across light:dark cycles in response to Fe availability, providing mechanistic understanding for the ability of diatoms to remain metabolically poised to respond quickly to Fe input and revealing strategies underlying their ecological success.
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http://dx.doi.org/10.1371/journal.pgen.1006490DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5156380PMC
December 2016

Genome and methylome of the oleaginous diatom reveal genetic flexibility toward a high lipid phenotype.

Biotechnol Biofuels 2016 25;9:258. Epub 2016 Nov 25.

Scripps Institution of Oceanography, University California San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0202 USA.

Background: Improvement in the performance of eukaryotic microalgae for biofuel and bioproduct production is largely dependent on characterization of metabolic mechanisms within the cell. The marine diatom which was originally identified in the Aquatic Species Program, is a promising strain of microalgae for large-scale production of biofuel and bioproducts, such as omega-3 fatty acids.

Results: We sequenced the nuclear genome and methylome of this oleaginous diatom to identify the genetic traits that enable substantial accumulation of triacylglycerol. The genome is comprised of highly methylated repetitive sequence, which does not significantly change under silicon starved lipid induction, and data further suggests the primary role of DNA methylation is to suppress DNA transposition. Annotation of pivotal glycolytic, lipid metabolism, and carbohydrate degradation processes reveal an expanded enzyme repertoire in  that would allow for an increased metabolic capacity toward triacylglycerol production. Identification of previously unidentified genes, including those involved in carbon transport and chitin metabolism, provide potential targets for genetic manipulation of carbon flux to further increase its lipid phenotype. New genetic tools were developed, bringing this organism on a par with other microalgae in terms of genetic manipulation and characterization approaches.

Conclusions: Functional annotation and detailed cross-species comparison of key carbon rich processes in highlights the importance of enzymatic subcellular compartmentation for regulation of carbon flux, which is often overlooked in photosynthetic microeukaryotes. The availability of the genome sequence, as well as advanced genetic manipulation tools enable further development of this organism for deployment in large-scale production systems.
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http://dx.doi.org/10.1186/s13068-016-0670-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5124317PMC
November 2016

Patterns of Transcript Abundance of Eukaryotic Biogeochemically-Relevant Genes in the Amazon River Plume.

PLoS One 2016 6;11(9):e0160929. Epub 2016 Sep 6.

University of South Florida College of Marine Science, St. Petersburg, FL, United States of America.

The Amazon River has the largest discharge of all rivers on Earth, and its complex plume system fuels a wide array of biogeochemical processes, across a large area of the western tropical North Atlantic. The plume thus stimulates microbial processes affecting carbon sequestration and nutrient cycles at a global scale. Chromosomal gene expression patterns of the 2.0 to 156 μm size-fraction eukaryotic microbial community were investigated in the Amazon River Plume, generating a robust dataset (more than 100 million mRNA sequences) that depicts the metabolic capabilities and interactions among the eukaryotic microbes. Combining classical oceanographic field measurements with metatranscriptomics yielded characterization of the hydrographic conditions simultaneous with a quantification of transcriptional activity and identity of the community. We highlight the patterns of eukaryotic gene expression for 31 biogeochemically significant gene targets hypothesized to be valuable within forecasting models. An advantage to this targeted approach is that the database of reference sequences used to identify the target genes was selectively constructed and highly curated optimizing taxonomic coverage, throughput, and the accuracy of annotations. A coastal diatom bloom highly expressed nitrate transporters and carbonic anhydrase presumably to support high growth rates and enhance uptake of low levels of dissolved nitrate and CO2. Diatom-diazotroph association (DDA: diatoms with nitrogen fixing symbionts) blooms were common when surface salinity was mesohaline and dissolved nitrate concentrations were below detection, and hence did not show evidence of nitrate utilization, suggesting they relied on ammonium transporters to aquire recently fixed nitrogen. These DDA blooms in the outer plume had rapid turnover of the photosystem D1 protein presumably caused by photodegradation under increased light penetration in clearer waters, and increased expression of silicon transporters as silicon became limiting. Expression of these genes, including carbonic anhydrase and transporters for nitrate and phosphate, were found to reflect the physiological status and biogeochemistry of river plume environments. These relatively stable patterns of eukaryotic transcript abundance occurred over modest spatiotemporal scales, with similarity observed in sample duplicates collected up to 2.45 km in space and 120 minutes in time. These results confirm the use of metatranscriptomics as a valuable tool to understand and predict microbial community function.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0160929PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5012681PMC
August 2017

Diversity and Expression of Bacterial Metacaspases in an Aquatic Ecosystem.

Front Microbiol 2016 6;7:1043. Epub 2016 Jul 6.

Science for Life Laboratory, Department of Ecology, Environment and Plant Sciences, Stockholm University Solna, Sweden.

Metacaspases are distant homologs of metazoan caspase proteases, implicated in stress response, and programmed cell death (PCD) in bacteria and phytoplankton. While the few previous studies on metacaspases have relied on cultured organisms and sequenced genomes, no studies have focused on metacaspases in a natural setting. We here present data from the first microbial community-wide metacaspase survey; performed by querying metagenomic and metatranscriptomic datasets from the brackish Baltic Sea, a water body characterized by pronounced environmental gradients and periods of massive cyanobacterial blooms. Metacaspase genes were restricted to ~4% of the bacteria, taxonomically affiliated mainly to Bacteroidetes, Alpha- and Betaproteobacteria and Cyanobacteria. The gene abundance was significantly higher in larger or particle-associated bacteria (>0.8 μm), and filamentous Cyanobacteria dominated metacaspase gene expression throughout the bloom season. Distinct seasonal expression patterns were detected for the three metacaspase genes in Nodularia spumigena, one of the main bloom-formers. Clustering of normalized gene expression in combination with analyses of genomic and assembly data suggest functional diversification of these genes, and possible roles of the metacaspase genes related to stress responses, i.e., sulfur metabolism in connection to oxidative stress, and nutrient stress induced cellular differentiation. Co-expression of genes encoding metacaspases and nodularin toxin synthesis enzymes was also observed in Nodularia spumigena. The study shows that metacaspases represent an adaptation of potentially high importance for several key organisms in the Baltic Sea, most prominently Cyanobacteria, and open up for further exploration of their physiological roles in microbes and assessment of their ecological impact in aquatic habitats.
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http://dx.doi.org/10.3389/fmicb.2016.01043DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4933709PMC
July 2016

Genetic Manipulation of Competition for Nitrate between Heterotrophic Bacteria and Diatoms.

Front Microbiol 2016 9;7:880. Epub 2016 Jun 9.

Integrative Oceanography Division, Scripps Institution of Oceanography, University of California San DiegoLa Jolla, CA, USA; Microbial and Environmental Genomics Group, J. Craig Venter InstituteLa Jolla, CA, USA.

Diatoms are a dominant group of eukaryotic phytoplankton that contribute substantially to global primary production and the cycling of important elements such as carbon and nitrogen. Heterotrophic bacteria, including members of the gammaproteobacteria, are commonly associated with diatom populations and may rely on them for organic carbon while potentially competing with them for other essential nutrients. Considering that bacterioplankton drive oceanic release of CO 2 (i.e., bacterial respiration) while diatoms drive ocean carbon sequestration vial the biological pump, the outcome of such competition could influence the direction and magnitude of carbon flux in the upper ocean. Nitrate availability is commonly a determining factor for the growth of diatom populations, particularly in coastal and upwelling regions. Diatoms as well as many bacterial species can utilize nitrate, however the ability of bacteria to compete for nitrate may be hindered by carbon limitation. Here we have developed a genetically tractable model system using the pennate diatom Phaeodactylum tricornutum and the widespread heterotrophic bacteria Alteromonas macleodii to examine carbon-nitrogen dynamics. While subsisting solely on P. tricornutum derived carbon, A. macleodii does not appear to be an effective competitor for nitrate, and may in fact benefit the diatom; particularly in stationary phase. However, allochthonous dissolved organic carbon addition in the form of pyruvate triggers A. macleodii proliferation and nitrate uptake, leading to reduced P. tricornutum growth. Nitrate reductase deficient mutants of A. macleodii (ΔnasA) do not exhibit such explosive growth and associated competitive ability in response to allochthonous carbon when nitrate is the sole nitrogen source, but could survive by utilizing solely P. tricornutum-derived nitrogen. Furthermore, allocthonous carbon addition enables wild-type A. macleodii to rescue nitrate reductase deficient P. tricornutum populations from nitrogen starvation, and RNA-seq transcriptomic evidence supports nitrogen-based interactions between diatoms and bacteria at the molecular level. This study provides key insights into the roles of carbon and nitrogen in phytoplankton-bacteria dynamics and lays the foundation for developing a mechanistic understanding of these interactions using co-culturing and genetic manipulation.
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http://dx.doi.org/10.3389/fmicb.2016.00880DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4899447PMC
July 2016

Spectrum of mitochondrial genomic variation and associated clinical presentation of prostate cancer in South African men.

Prostate 2016 Mar 10;76(4):349-58. Epub 2015 Dec 10.

J. Craig Venter Institute, La Jolla, California.

Background: Prostate cancer incidence and mortality rates are significantly increased in African-American men, but limited studies have been performed within Sub-Saharan African populations. As mitochondria control energy metabolism and apoptosis we speculate that somatic mutations within mitochondrial genomes are candidate drivers of aggressive prostate carcinogenesis.

Methods: We used matched blood and prostate tissue samples from 87 South African men (77 with African ancestry) to perform deep sequencing of complete mitochondrial genomes. Clinical presentation was biased toward aggressive disease (Gleason score >7, 64%), and compared with men without prostate cancer either with or without benign prostatic hyperplasia.

Results: We identified 144 somatic mtDNA single nucleotide variants (SNVs), of which 80 were observed in 39 men presenting with aggressive disease. Both the number and frequency of somatic mtDNA SNVs were associated with higher pathological stage.

Conclusions: Besides doubling the total number of somatic PCa-associated mitochondrial genome mutations identified to date, we associate mutational load with aggressive prostate cancer status in men of African ancestry.
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http://dx.doi.org/10.1002/pros.23126DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4832339PMC
March 2016

Phytoplankton-bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge.

Proc Natl Acad Sci U S A 2015 Aug 28;112(32):9938-43. Epub 2015 Jul 28.

Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA 92037; Integrative Oceanography Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92037;

Southern Ocean primary productivity plays a key role in global ocean biogeochemistry and climate. At the Southern Ocean sea ice edge in coastal McMurdo Sound, we observed simultaneous cobalamin and iron limitation of surface water phytoplankton communities in late Austral summer. Cobalamin is produced only by bacteria and archaea, suggesting phytoplankton-bacterial interactions must play a role in this limitation. To characterize these interactions and investigate the molecular basis of multiple nutrient limitation, we examined transitions in global gene expression over short time scales, induced by shifts in micronutrient availability. Diatoms, the dominant primary producers, exhibited transcriptional patterns indicative of co-occurring iron and cobalamin deprivation. The major contributor to cobalamin biosynthesis gene expression was a gammaproteobacterial population, Oceanospirillaceae ASP10-02a. This group also contributed significantly to metagenomic cobalamin biosynthesis gene abundance throughout Southern Ocean surface waters. Oceanospirillaceae ASP10-02a displayed elevated expression of organic matter acquisition and cell surface attachment-related genes, consistent with a mutualistic relationship in which they are dependent on phytoplankton growth to fuel cobalamin production. Separate bacterial groups, including Methylophaga, appeared to rely on phytoplankton for carbon and energy sources, but displayed gene expression patterns consistent with iron and cobalamin deprivation. This suggests they also compete with phytoplankton and are important cobalamin consumers. Expression patterns of siderophore- related genes offer evidence for bacterial influences on iron availability as well. The nature and degree of this episodic colimitation appear to be mediated by a series of phytoplankton-bacterial interactions in both positive and negative feedback loops.
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http://dx.doi.org/10.1073/pnas.1501615112DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4538660PMC
August 2015

Genomes and gene expression across light and productivity gradients in eastern subtropical Pacific microbial communities.

ISME J 2015 May 21;9(5):1076-92. Epub 2014 Oct 21.

1] Microbial and Environmental Genomics Group, J. Craig Venter Institute, La Jolla, CA, USA [2] Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA, USA.

Transitions in community genomic features and biogeochemical processes were examined in surface and subsurface chlorophyll maximum (SCM) microbial communities across a trophic gradient from mesotrophic waters near San Diego, California to the oligotrophic Pacific. Transect end points contrasted in thermocline depth, rates of nitrogen and CO2 uptake, new production and SCM light intensity. Relative to surface waters, bacterial SCM communities displayed greater genetic diversity and enrichment in putative sulfur oxidizers, multiple actinomycetes, low-light-adapted Prochlorococcus and cell-associated viruses. Metagenomic coverage was not correlated with transcriptional activity for several key taxa within Bacteria. Low-light-adapted Prochlorococcus, Synechococcus, and low abundance gamma-proteobacteria enriched in the>3.0-μm size fraction contributed disproportionally to global transcription. The abundance of these groups also correlated with community functions, such as primary production or nitrate uptake. In contrast, many of the most abundant bacterioplankton, including SAR11, SAR86, SAR112 and high-light-adapted Prochlorococcus, exhibited low levels of transcriptional activity and were uncorrelated with rate processes. Eukaryotes such as Haptophytes and non-photosynthetic Aveolates were prevalent in surface samples while Mamielles and Pelagophytes dominated the SCM. Metatranscriptomes generated with ribosomal RNA-depleted mRNA (total mRNA) coupled to in vitro polyadenylation compared with polyA-enriched mRNA revealed a trade-off in detection eukaryotic organelle and eukaryotic nuclear origin transcripts, respectively. Gene expression profiles of SCM eukaryote populations, highly similar in sequence identity to the model pelagophyte Pelagomonas sp. CCMP1756, suggest that pelagophytes are responsible for a majority of nitrate assimilation within the SCM.
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http://dx.doi.org/10.1038/ismej.2014.198DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4410273PMC
May 2015

Functional tradeoffs underpin salinity-driven divergence in microbial community composition.

PLoS One 2014 27;9(2):e89549. Epub 2014 Feb 27.

Department of Ecology, Environment and Plant Sciences, Stockholm University, Stockholm, Sweden.

Bacterial community composition and functional potential change subtly across gradients in the surface ocean. In contrast, while there are significant phylogenetic divergences between communities from freshwater and marine habitats, the underlying mechanisms to this phylogenetic structuring yet remain unknown. We hypothesized that the functional potential of natural bacterial communities is linked to this striking divide between microbiomes. To test this hypothesis, metagenomic sequencing of microbial communities along a 1,800 km transect in the Baltic Sea area, encompassing a continuous natural salinity gradient from limnic to fully marine conditions, was explored. Multivariate statistical analyses showed that salinity is the main determinant of dramatic changes in microbial community composition, but also of large scale changes in core metabolic functions of bacteria. Strikingly, genetically and metabolically different pathways for key metabolic processes, such as respiration, biosynthesis of quinones and isoprenoids, glycolysis and osmolyte transport, were differentially abundant at high and low salinities. These shifts in functional capacities were observed at multiple taxonomic levels and within dominant bacterial phyla, while bacteria, such as SAR11, were able to adapt to the entire salinity gradient. We propose that the large differences in central metabolism required at high and low salinities dictate the striking divide between freshwater and marine microbiomes, and that the ability to inhabit different salinity regimes evolved early during bacterial phylogenetic differentiation. These findings significantly advance our understanding of microbial distributions and stress the need to incorporate salinity in future climate change models that predict increased levels of precipitation and a reduction in salinity.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0089549PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3937345PMC
October 2014

Lineage specific gene family enrichment at the microscale in marine systems.

Curr Opin Microbiol 2013 Oct;16(5):605-17

Recent advances in metagenomics have generated numerous insights related to the cell biology, ecology, evolution, and biogeochemistry of microbial life in the ocean. Notably, advances in single cell genomics (SCG), fluorescence activated cell sorting (FACS) capture of specific populations and metagenomic assembly are providing valuable information related to within and between lineage genomic content. Improved reference genome databases have assisted biogeographic studies of particular taxa, including in some cases different ecotypes. Several studies targeting picoplankton, associated with various particle size classes, have begun to define contrasting trends in gene family evolution between free-living compared to particle associated microbes. Also viruses and eukaryotic microbes are increasingly considered in metagenomic studies and specific associations between viruses, bacteria, archaea, and eukaryotic microbes are emerging.
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http://dx.doi.org/10.1016/j.mib.2013.10.001DOI Listing
October 2013

Metagenomic exploration of viruses throughout the Indian Ocean.

PLoS One 2012 17;7(10):e42047. Epub 2012 Oct 17.

Microbial and Environmental Genomics, J. Craig Venter Institute, San Diego, California, USA.

The characterization of global marine microbial taxonomic and functional diversity is a primary goal of the Global Ocean Sampling Expedition. As part of this study, 19 water samples were collected aboard the Sorcerer II sailing vessel from the southern Indian Ocean in an effort to more thoroughly understand the lifestyle strategies of the microbial inhabitants of this ultra-oligotrophic region. No investigations of whole virioplankton assemblages have been conducted on waters collected from the Indian Ocean or across multiple size fractions thus far. Therefore, the goals of this study were to examine the effect of size fractionation on viral consortia structure and function and understand the diversity and functional potential of the Indian Ocean virome. Five samples were selected for comprehensive metagenomic exploration; and sequencing was performed on the microbes captured on 3.0-, 0.8- and 0.1 µm membrane filters as well as the viral fraction (<0.1 µm). Phylogenetic approaches were also used to identify predicted proteins of viral origin in the larger fractions of data from all Indian Ocean samples, which were included in subsequent metagenomic analyses. Taxonomic profiling of viral sequences suggested that size fractionation of marine microbial communities enriches for specific groups of viruses within the different size classes and functional characterization further substantiated this observation. Functional analyses also revealed a relative enrichment for metabolic proteins of viral origin that potentially reflect the physiological condition of host cells in the Indian Ocean including those involved in nitrogen metabolism and oxidative phosphorylation. A novel classification method, MGTAXA, was used to assess virus-host relationships in the Indian Ocean by predicting the taxonomy of putative host genera, with Prochlorococcus, Acanthochlois and members of the SAR86 cluster comprising the most abundant predictions. This is the first study to holistically explore virioplankton dynamics across multiple size classes and provides unprecedented insight into virus diversity, metabolic potential and virus-host interactions.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0042047PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3474794PMC
April 2013

Influence of nutrients and currents on the genomic composition of microbes across an upwelling mosaic.

ISME J 2012 Jul 26;6(7):1403-14. Epub 2012 Jan 26.

Microbial and Environmental Genomics, J Craig Venter Institute, San Diego, CA, USA.

Metagenomic data sets were generated from samples collected along a coastal to open ocean transect between Southern California Bight and California Current waters during a seasonal upwelling event, providing an opportunity to examine the impact of episodic pulses of cold nutrient-rich water into surface ocean microbial communities. The data set consists of ~5.8 million predicted proteins across seven sites, from three different size classes: 0.1-0.8, 0.8-3.0 and 3.0-200.0 μm. Taxonomic and metabolic analyses suggest that sequences from the 0.1-0.8 μm size class correlated with their position along the upwelling mosaic. However, taxonomic profiles of bacteria from the larger size classes (0.8-200 μm) were less constrained by habitat and characterized by an increase in Cyanobacteria, Bacteroidetes, Flavobacteria and double-stranded DNA viral sequences. Functional annotation of transmembrane proteins indicate that sites comprised of organisms with small genomes have an enrichment of transporters with substrate specificities for amino acids, iron and cadmium, whereas organisms with larger genomes have a higher percentage of transporters for ammonium and potassium. Eukaryotic-type glutamine synthetase (GS) II proteins were identified and taxonomically classified as viral, most closely related to the GSII in Mimivirus, suggesting that marine Mimivirus-like particles may have played a role in the transfer of GSII gene functions. Additionally, a Planctomycete bloom was sampled from one upwelling site providing a rare opportunity to assess the genomic composition of a marine Planctomycete population. The significant correlations observed between genomic properties, community structure and nutrient availability provide insights into habitat-driven dynamics among oligotrophic versus upwelled marine waters adjoining each other spatially.
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http://dx.doi.org/10.1038/ismej.2011.201DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3379637PMC
July 2012

Evolution and metabolic significance of the urea cycle in photosynthetic diatoms.

Nature 2011 May;473(7346):203-7

J. Craig Venter Institute, San Diego, California 92121, USA.

Diatoms dominate the biomass of phytoplankton in nutrient-rich conditions and form the basis of some of the world's most productive marine food webs. The diatom nuclear genome contains genes with bacterial and plastid origins as well as genes of the secondary endosymbiotic host (the exosymbiont), yet little is known about the relative contribution of each gene group to diatom metabolism. Here we show that the exosymbiont-derived ornithine-urea cycle, which is similar to that of metazoans but is absent in green algae and plants, facilitates rapid recovery from prolonged nitrogen limitation. RNA-interference-mediated knockdown of a mitochondrial carbamoyl phosphate synthase impairs the response of nitrogen-limited diatoms to nitrogen addition. Metabolomic analyses indicate that intermediates in the ornithine-urea cycle are particularly depleted and that both the tricarboxylic acid cycle and the glutamine synthetase/glutamate synthase cycles are linked directly with the ornithine-urea cycle. Several other depleted metabolites are generated from ornithine-urea cycle intermediates by the products of genes laterally acquired from bacteria. This metabolic coupling of bacterial- and exosymbiont-derived proteins seems to be fundamental to diatom physiology because the compounds affected include the major diatom osmolyte proline and the precursors for long-chain polyamines required for silica precipitation during cell wall formation. So far, the ornithine-urea cycle is only known for its essential role in the removal of fixed nitrogen in metazoans. In diatoms, this cycle serves as a distribution and repackaging hub for inorganic carbon and nitrogen and contributes significantly to the metabolic response of diatoms to episodic nitrogen availability. The diatom ornithine-urea cycle therefore represents a key pathway for anaplerotic carbon fixation into nitrogenous compounds that are essential for diatom growth and for the contribution of diatoms to marine productivity.
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http://dx.doi.org/10.1038/nature10074DOI Listing
May 2011

A rapid fingerprinting approach to distinguish between closely related strains of Shewanella.

J Microbiol Methods 2011 Jul 6;86(1):62-8. Epub 2011 Apr 6.

Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089, USA.

One of the big operational problems facing laboratories today is the ability to rapidly distinguish between strains of bacteria that, while physiologically distinct, are nearly impossible to separate based on 16S rRNA gene sequence differences. Here we demonstrate that ITS-DGGE provides a convenient approach to distinguishing between closely related strains of Shewanella, some of which were impossible to separate and identify by 16 rRNA gene sequence alone. Examined Shewanella genomes contain 8-11 copies of rrn (ribosomal RNA gene) operons, and variable size and sequence of 16S-23S ITS (intergenic transcribed spacer) regions which result in distinct ITS-DGGE profiles. Phylogenetic constructions based on ITS are congruent with the genomic trees generated from concatenated core genes as well as with those based on conserved indels, suggesting that ITS patterns appear to be linked with evolutionary lineages and physiology. In addition, three new Shewanella strains (MFC 2, MFC 6, and MFC 14) were isolated from microbial fuel cells enriched from wastewater sludge and identified by ITS-DGGE. Subsequent physiological and electrochemical studies of the three isolates confirmed that each strain is phenotypically/genotypically distinct. Thus, this study validates ITS-DGGE as a quick fingerprint approach to identifying and distinguishing between closely related but novel Shewanella ecotypes.
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http://dx.doi.org/10.1016/j.mimet.2011.03.017DOI Listing
July 2011

Genomic and functional adaptation in surface ocean planktonic prokaryotes.

Nature 2010 Nov;468(7320):60-6

J. Craig Venter Institute, Rockville, Maryland 20850, USA.

The understanding of marine microbial ecology and metabolism has been hampered by the paucity of sequenced reference genomes. To this end, we report the sequencing of 137 diverse marine isolates collected from around the world. We analysed these sequences, along with previously published marine prokaryotic genomes, in the context of marine metagenomic data, to gain insights into the ecology of the surface ocean prokaryotic picoplankton (0.1-3.0 μm size range). The results suggest that the sequenced genomes define two microbial groups: one composed of only a few taxa that are nearly always abundant in picoplanktonic communities, and the other consisting of many microbial taxa that are rarely abundant. The genomic content of the second group suggests that these microbes are capable of slow growth and survival in energy-limited environments, and rapid growth in energy-rich environments. By contrast, the abundant and cosmopolitan picoplanktonic prokaryotes for which there is genomic representation have smaller genomes, are probably capable of only slow growth and seem to be relatively unable to sense or rapidly acclimate to energy-rich conditions. Their genomic features also lead us to propose that one method used to avoid predation by viruses and/or bacterivores is by means of slow growth and the maintenance of low biomass.
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http://dx.doi.org/10.1038/nature09530DOI Listing
November 2010

Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton.

Proc Natl Acad Sci U S A 2010 Aug 28;107(33):14679-84. Epub 2010 Jul 28.

Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039, USA.

Among eukaryotes, four major phytoplankton lineages are responsible for marine photosynthesis; prymnesiophytes, alveolates, stramenopiles, and prasinophytes. Contributions by individual taxa, however, are not well known, and genomes have been analyzed from only the latter two lineages. Tiny "picoplanktonic" members of the prymnesiophyte lineage have long been inferred to be ecologically important but remain poorly characterized. Here, we examine pico-prymnesiophyte evolutionary history and ecology using cultivation-independent methods. 18S rRNA gene analysis showed pico-prymnesiophytes belonged to broadly distributed uncultivated taxa. Therefore, we used targeted metagenomics to analyze uncultured pico-prymnesiophytes sorted by flow cytometry from subtropical North Atlantic waters. The data reveal a composite nuclear-encoded gene repertoire with strong green-lineage affiliations, which contrasts with the evolutionary history indicated by the plastid genome. Measured pico-prymnesiophyte growth rates were rapid in this region, resulting in primary production contributions similar to the cyanobacterium Prochlorococcus. On average, pico-prymnesiophytes formed 25% of global picophytoplankton biomass, with differing contributions in five biogeographical provinces spanning tropical to subpolar systems. Elements likely contributing to success include high gene density and genes potentially involved in defense and nutrient uptake. Our findings have implications reaching beyond pico-prymnesiophytes, to the prasinophytes and stramenopiles. For example, prevalence of putative Ni-containing superoxide dismutases (SODs), instead of Fe-containing SODs, seems to be a common adaptation among eukaryotic phytoplankton for reducing Fe quotas in low-Fe modern oceans. Moreover, highly mosaic gene repertoires, although compositionally distinct for each major eukaryotic lineage, now seem to be an underlying facet of successful marine phytoplankton.
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http://dx.doi.org/10.1073/pnas.1001665107DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2930470PMC
August 2010

Alignment of phylogenetically unambiguous indels in Shewanella.

Authors:
John P McCrow

J Comput Biol 2009 Nov;16(11):1517-28

J Craig Venter Institute, San Diego, CA 92121, USA.

High levels of alignment errors associated with gaps have generally meant their exclusion from phylogenetic analysis. Conserved inserts and deletions (indels) may in some cases be less subject to errors than amino acid substitutions for inferring the history of genomes and identifying recently laterally transferred genes, but alignment error near gaps must be evaluated prior to using indels as phylogenetic characters. A method is presented for evaluating the phylogenetic unambiguity of gaps in multiple sequence alignments by allowing a defined amount of pairwise alignment ambiguity. This work considers the bacterial genus Shewanella, which is of particular interest for applications of bioremediation and environmental engineering. Understanding the genetic history of these species is vital for these applications. A set of pairwise dynamic programming alignments is constructed to test positions in multiple alignments for phylogenetic unambiguity, and a whole genome scan is done on protein sequences from 11 sequenced species of the bacterial genus Shewanella. The splits defined by phylogenetically unambiguous indels are then used as characters for phylogenetic analysis, and results are compared to whole genome Maximum Likelihood phylogeny. A comparable description of the history of the species is found, as well as a set of lateral gene transfer candidates undetectable by traditional analysis of amino acid substitutions. This analysis is applicable to other taxonomic units at all levels and has the potential to allow cataloging of clear genome-wide phylogenetic markers for taxonomic profiling down to the species level.
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http://dx.doi.org/10.1089/cmb.2009.0188DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3154395PMC
November 2009