Webb Eric A

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Eric A

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  • Article
    Irreversibly increased nitrogen fixation in Trichodesmium experimentally adapted to elevated carbon dioxide
    (Nature Publishing Group, 2015-09-01) Hutchins, David A. ; Walworth, Nathan G. ; Webb, Eric A. ; Saito, Mak A. ; Moran, Dawn M. ; McIlvin, Matthew R. ; Gale, Jasmine ; Fu, Fei-Xue
    Nitrogen fixation rates of the globally distributed, biogeochemically important marine cyanobacterium Trichodesmium increase under high carbon dioxide (CO2) levels in short-term studies due to physiological plasticity. However, its long-term adaptive responses to ongoing anthropogenic CO2 increases are unknown. Here we show that experimental evolution under extended selection at projected future elevated CO2 levels results in irreversible, large increases in nitrogen fixation and growth rates, even after being moved back to lower present day CO2 levels for hundreds of generations. This represents an unprecedented microbial evolutionary response, as reproductive fitness increases acquired in the selection environment are maintained after returning to the ancestral environment. Constitutive rate increases are accompanied by irreversible shifts in diel nitrogen fixation patterns, and increased activity of a potentially regulatory DNA methyltransferase enzyme. High CO2-selected cell lines also exhibit increased phosphorus-limited growth rates, suggesting a potential advantage for this keystone organism in a more nutrient-limited, acidified future ocean.
  • Article
    Characterization of Trichodesmium spp. by genetic techniques
    (American Society for Microbiology, 2002-05) Orcutt, K. M. ; Rasmussen, U. ; Webb, Eric A. ; Waterbury, John B. ; Gundersen, K. ; Bergman, B.
    The genetic diversity of Trichodesmium spp. from natural populations (off Bermuda in the Sargasso Sea and off North Australia in the Arafura and Coral Seas) and of culture isolates from two regions (Sargasso Sea and Indian Ocean) was investigated. Three independent techniques were used, including a DNA fingerprinting method based on a highly iterated palindrome (HIP1), denaturing gradient gel electrophoresis of a hetR fragment, and sequencing of the internal transcribed spacer (ITS) of the 16S-23S rDNA region. Low genetic diversity was observed in natural populations of Trichodesmium spp. from the two hemispheres. Culture isolates of Trichodesmium thiebautii, Trichodesmium hildebrandtii, Trichodesmium tenue, and Katagnymene spiralis displayed remarkable similarity when these techniques were used, suggesting that K. spiralis is very closely related to the genus Trichodesmium. The largest genetic variation was found between Trichodesmium erythraeum and all other species of Trichodesmium, including a species of Katagnymene. Our data obtained with all three techniques suggest that there are two major clades of Trichodesmium spp. The HIP1 fingerprinting and ITS sequence analyses allowed the closely related species to be distinguished. This is the first report of the presence of HIP1 in marine cyanobacteria.
  • Dataset
    POC and PON from Trichodesmium colonies from RV/Atlantic cruise AT39-05, Feb-Mar 2018
    (Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2020-05-04) Hutchins, David A. ; Webb, Eric A
    POC and PON from Trichodesmium colonies from RV/Atlantic cruise AT39-05, Feb-Mar 2018. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/766394
  • Dataset
    Synechococcus counts determined by epifluorescent microscopy from samples collected on R/V Atlantis cruise AT15-61 in the Eastern Tropical South Pacific in 2010 (Syne_ETSP project)
    (Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2019-08-01) Webb, Eric A ; Sohm, Jill
    Synechococcus counts determined by epifluorescent microscopy from samples collected on R/V Atlantis cruise AT15-61 in the Eastern Tropical South Pacific in 2010. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/3765
  • Article
    Lesions in gshA (encoding gamma -L-glutamyl-L-cysteine synthetase) prevent aerobic synthesis of thiamine in Salmonella enterica serovar Typhimurium LT2
    (American Society for Microbiology, 2000-09) Gralnick, Jeffrey ; Webb, Eric A. ; Beck, Brian ; Downs, Diana
    Thiamine pyrophosphate is an essential cofactor that is synthesized de novo in Salmonella enterica serovar Typhimurium and other bacteria. In addition to genes encoding enzymes in the biosynthetic pathway, mutations in other metabolic loci have been shown to prevent thiamine synthesis. The latter loci identify the integration of the thiamine biosynthetic pathway with other metabolic processes and can be uncovered when thiamine biosynthesis is challenged. Mutations in gshA, encoding gamma -L-glutamyl-L-cysteine synthetase, prevent the synthesis of glutathione, the major free thiol in the cell, and are shown here to result in a thiamine auxotrophy in some of the strains tested, including S. enterica LT2. Phenotypic characterization of the gshA mutants indicated they were similar enough to apbC and apbE mutants to warrant the definition of a class of mutants unified by (i) a requirement for both the hydroxymethyl pyrimidine (HMP) and thiazole (THZ) moiety of thiamine, (ii) the ability of L-tryosine to satisfy the THZ requirement, (iii) suppression of the thiamine requirement by anaerobic growth, and (iv) suppression by a second-site mutation at a single locus. Genetic data indicated that a defective ThiH generates the THZ requirement in these strains, and we suggest this defect is due to a reduced ability to repair a critical [Fe-S] cluster.
  • Article
    Distribution and diversity of natural product genes in marine and freshwater cyanobacterial cultures and genomes
    (American Society for Microbiology, 2005-11) Ehrenreich, Ian M. ; Waterbury, John B. ; Webb, Eric A.
    Natural products are a functionally diverse class of biochemically synthesized compounds, which include antibiotics, toxins, and siderophores. In this paper, we describe both the detection of natural product activities and the sequence identification of gene fragments from two molecular systems that have previously been implicated in natural product production, i.e., nonribosomal peptide synthetases (NRPSs) and modular polyketide synthases (PKSs), in diverse marine and freshwater cyanobacterial cultures. Using degenerate PCR and the sequencing of cloned products, we show that NRPSs and PKSs are common among the cyanobacteria tested. Our molecular data, when combined with genomic searches of finished and progressing cyanobacterial genomes, demonstrate that not all cyanobacteria contain NRPS and PKS genes and that the filamentous and heterocystous cyanobacteria are the richest sources of these genes and the most likely sources of novel natural products within the phylum. In addition to validating the use of degenerate primers for the identification of PKS and NRPS genes in cyanobacteria, this study also defines numerous gene fragments that will be useful as probes for future studies of the synthesis of natural products in cyanobacteria. Phylogenetic analyses of the cyanobacterial NRPS and PKS fragments sequenced in this study, as well as those from the cyanobacterial genome projects, demonstrate that there is remarkable diversity and likely novelty of these genes within the cyanobacteria. These results underscore the potential variety of novel products being produced by these ubiquitous organisms.
  • Article
    Mariprofundus ferrooxydans PV-1 the First Genome of a Marine Fe(II) Oxidizing Zetaproteobacterium
    (Public Library of Science, 2011-09-23) Singer, Esther ; Emerson, David ; Webb, Eric A. ; Barco, Roman A. ; Kuenen, J. Gijs ; Nelson, William C. ; Chan, Clara S. ; Comolli, Luis R. ; Ferriera, Steve ; Johnson, Justin ; Heidelberg, John F. ; Edwards, Katrina J.
    Mariprofundus ferrooxydans PV-1 has provided the first genome of the recently discovered Zetaproteobacteria subdivision. Genome analysis reveals a complete TCA cycle, the ability to fix CO2, carbon-storage proteins and a sugar phosphotransferase system (PTS). The latter could facilitate the transport of carbohydrates across the cell membrane and possibly aid in stalk formation, a matrix composed of exopolymers and/or exopolysaccharides, which is used to store oxidized iron minerals outside the cell. Two-component signal transduction system genes, including histidine kinases, GGDEF domain genes, and response regulators containing CheY-like receivers, are abundant and widely distributed across the genome. Most of these are located in close proximity to genes required for cell division, phosphate uptake and transport, exopolymer and heavy metal secretion, flagellar biosynthesis and pilus assembly suggesting that these functions are highly regulated. Similar to many other motile, microaerophilic bacteria, genes encoding aerotaxis as well as antioxidant functionality (e.g., superoxide dismutases and peroxidases) are predicted to sense and respond to oxygen gradients, as would be required to maintain cellular redox balance in the specialized habitat where M. ferrooxydans resides. Comparative genomics with other Fe(II) oxidizing bacteria residing in freshwater and marine environments revealed similar content, synteny, and amino acid similarity of coding sequences potentially involved in Fe(II) oxidation, signal transduction and response regulation, oxygen sensation and detoxification, and heavy metal resistance. This study has provided novel insights into the molecular nature of Zetaproteobacteria.
  • Article
    Iron stress in open-ocean cyanobacteria (Synechococcus, Trichodesmium, and Crocosphaera spp.) : identification of the IdiA protein
    (American Society for Microbiology, 2001-12) Webb, Eric A. ; Moffett, James W. ; Waterbury, John B.
    Cyanobacteria are prominent constituents of the marine biosphere that account for a significant percentage of oceanic primary productivity. In an effort to resolve how open-ocean cyanobacteria persist in regions where the Fe concentration is thought to be limiting their productivity, we performed a number of Fe stress experiments on axenic cultures of marine Synechococcus spp., Crocosphaera sp., and Trichodesmium sp. Through this work, we determined that all of these marine cyanobacteria mount adaptive responses to Fe stress, which resulted in the induction and/or repression of several proteins. We have identified one of the Fe stress-induced proteins as an IdiA homologue. Genomic observations and laboratory data presented herein from open-ocean Synechococcus spp. are consistent with IdiA having a role in cellular Fe scavenging. Our data indicate that IdiA may make an excellent marker for Fe stress in open-ocean cyanobacterial field populations. By determining how these microorganisms respond to Fe stress, we will gain insight into how and when this important trace element can limit their growth in situ. This knowledge will greatly increase our understanding of how marine Fe cycling impacts oceanic processes, such as carbon and nitrogen fixation.
  • Preprint
    Comment on “The complex effects of ocean acidification on the prominent N2-fixing cyanobacterium Trichodesmium”
    ( 2017-08) Hutchins, David A. ; Fu, Feixue ; Walworth, Nathan G. ; Lee, Michael D. ; Saito, Mak A. ; Webb, Eric A.
    Hong et al. (Reports, 5 May 2017, p. 527) suggested that previous studies of the biogeochemically significant marine cyanobacterium Trichodesmium showing increased growth and nitrogen fixation at projected future high CO2 levels suffered from ammonia or copper toxicity. They reported that these rates instead decrease at high CO2 when contamination is alleviated. We present and discuss results of multiple published studies refuting this toxicity hypothesis.
  • Article
    Microbial functional diversity across biogeochemical provinces in the central Pacific Ocean
    (National Academy of Sciences, 2022-09-13) Saunders, Jaclyn K. ; McIlvin, Matthew R. ; Dupont, Christopher L. ; Kaul, Drishti ; Moran, Dawn M. ; Horner, Tristan J. ; Laperriere, Sarah ; Webb, Eric A. ; Bosak, Tanja ; Santoro, Alyson E. ; Saito, Mak A.
    Enzymes catalyze key reactions within Earth’s life-sustaining biogeochemical cycles. Here, we use metaproteomics to examine the enzymatic capabilities of the microbial community (0.2 to 3 µm) along a 5,000-km-long, 1-km-deep transect in the central Pacific Ocean. Eighty-five percent of total protein abundance was of bacterial origin, with Archaea contributing 1.6%. Over 2,000 functional KEGG Ontology (KO) groups were identified, yet only 25 KO groups contributed over half of the protein abundance, simultaneously indicating abundant key functions and a long tail of diverse functions. Vertical attenuation of individual proteins displayed stratification of nutrient transport, carbon utilization, and environmental stress. The microbial community also varied along horizontal scales, shaped by environmental features specific to the oligotrophic North Pacific Subtropical Gyre, the oxygen-depleted Eastern Tropical North Pacific, and nutrient-rich equatorial upwelling. Some of the most abundant proteins were associated with nitrification and C1 metabolisms, with observed interactions between these pathways. The oxidoreductases nitrite oxidoreductase (NxrAB), nitrite reductase (NirK), ammonia monooxygenase (AmoABC), manganese oxidase (MnxG), formate dehydrogenase (FdoGH and FDH), and carbon monoxide dehydrogenase (CoxLM) displayed distributions indicative of biogeochemical status such as oxidative or nutritional stress, with the potential to be more sensitive than chemical sensors. Enzymes that mediate transformations of atmospheric gases like CO, CO2, NO, methanethiol, and methylamines were most abundant in the upwelling region. We identified hot spots of biochemical transformation in the central Pacific Ocean, highlighted previously understudied metabolic pathways in the environment, and provided rich empirical data for biogeochemical models critical for forecasting ecosystem response to climate change.
  • Article
    Functional genomics and phylogenetic evidence suggest genus-wide cobalamin production by the globally distributed marine nitrogen fixer Trichodesmium
    (Frontiers Media, 2018-02-13) Walworth, Nathan G. ; Lee, Michael D. ; Suffridge, Christopher ; Qu, Pingping ; Fu, Fei-Xue ; Saito, Mak A. ; Webb, Eric A. ; Sañudo-Wilhelmy, Sergio A. ; Hutchins, David A.
    Only select prokaryotes can biosynthesize vitamin B12 (i.e., cobalamins), but these organic co-enzymes are required by all microbial life and can be vanishingly scarce across extensive ocean biomes. Although global ocean genome data suggest cyanobacteria to be a major euphotic source of cobalamins, recent studies have highlighted that >95% of cyanobacteria can only produce a cobalamin analog, pseudo-B12, due to the absence of the BluB protein that synthesizes the α ligand 5,6-dimethylbenzimidizole (DMB) required to biosynthesize cobalamins. Pseudo-B12 is substantially less bioavailable to eukaryotic algae, as only certain taxa can intracellularly remodel it to one of the cobalamins. Here we present phylogenetic, metagenomic, transcriptomic, proteomic, and chemical analyses providing multiple lines of evidence that the nitrogen-fixing cyanobacterium Trichodesmium transcribes and translates the biosynthetic, cobalamin-requiring BluB enzyme. Phylogenetic evidence suggests that the Trichodesmium DMB biosynthesis gene, bluB, is of ancient origin, which could have aided in its ecological differentiation from other nitrogen-fixing cyanobacteria. Additionally, orthologue analyses reveal two genes encoding iron-dependent B12 biosynthetic enzymes (cbiX and isiB), suggesting that iron availability may be linked not only to new nitrogen supplies from nitrogen fixation, but also to B12 inputs by Trichodesmium. These analyses suggest that Trichodesmium contains the genus-wide genomic potential for a previously unrecognized role as a source of cobalamins, which may prove to considerably impact marine biogeochemical cycles.
  • Article
    Nitrogen fixation in the South Atlantic Gyre and the Benguela Upwelling System
    (American Geophysical Union, 2011-08-27) Sohm, Jill A. ; Hilton, Jason A. ; Noble, Abigail E. ; Zehr, Jonathan P. ; Saito, Mak A. ; Webb, Eric A.
    Dinitrogen (N2) fixation is recognized as an important input of new nitrogen (N) to the open ocean gyres, contributing to the export of organic matter from surface waters. However, very little N2-fixation research has focused on the South Atlantic Gyre, where dust deposition of iron (Fe), an important micronutrient for diazotrophs, is seasonally low. Recent modeling efforts suggest that N2-fixation may in fact be closely coupled to, and greatest in, areas of denitrification, as opposed to the oceanic gyres. One of these areas, the Benguela Upwelling System, lies to the east of the South Atlantic Gyre. In this study we show that N2-fixation in surface waters across the South Atlantic Gyre was low overall (<1.5 nmol N l−1 d−1) with highest rates seen in or near the Benguela Upwelling System (up to ∼8 nmol N l−1 d−1). Surface water dissolved Fe (dFe) concentrations were very low in the gyre (∼0.3 nM or lower), while soluble reactive phosphorus (SRP) concentrations were relatively high (∼0.15 μM). N2-fixation rates across the entire sampling area were significantly positively correlated to dFe, but also to SRP and NO3−. Thus, high NO3− concentrations did not exclude N2-fixation in the upwelling region, which provides evidence that N2-fixation may be occurring in previously unrecognized waters, specifically near denitrification zones. However the gene encoding for a nitrogenase component (nifH) was not detected from known diazotrophs at some stations in or near the upwelling where N2-fixation was greatest, suggesting the presence of unknown diazotrophs in these waters.
  • Article
    Mechanisms of increased Trichodesmium fitness under iron and phosphorus co-limitation in the present and future ocean
    (Nature Publishing Group, 2016-06-27) Walworth, Nathan G. ; Fu, Fei-Xue ; Webb, Eric A. ; Saito, Mak A. ; Moran, Dawn M. ; Mcllvin, Matthew R. ; Lee, Michael D. ; Hutchins, David A.
    Nitrogen fixation by cyanobacteria supplies critical bioavailable nitrogen to marine ecosystems worldwide; however, field and lab data have demonstrated it to be limited by iron, phosphorus and/or CO2. To address unknown future interactions among these factors, we grew the nitrogen-fixing cyanobacterium Trichodesmium for 1 year under Fe/P co-limitation following 7 years of both low and high CO2 selection. Fe/P co-limited cell lines demonstrated a complex cellular response including increased growth rates, broad proteome restructuring and cell size reductions relative to steady-state growth limited by either Fe or P alone. Fe/P co-limitation increased abundance of a protein containing a conserved domain previously implicated in cell size regulation, suggesting a similar role in Trichodesmium. Increased CO2 further induced nutrient-limited proteome shifts in widespread core metabolisms. Our results thus suggest that N2-fixing microbes may be significantly impacted by interactions between elevated CO2 and nutrient limitation, with broad implications for global biogeochemical cycles in the future ocean.
  • Dataset
    Nitrogen and carbon fixation rates from Trichodesmium colonies from RV/Atlantic cruise AT39-05, Feb-Mar 2018
    (Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2020-05-04) Hutchins, David A. ; Webb, Eric A
    Nitrogen and carbon fixation rates from Trichodesmium colonies from RV/Atlantic cruise AT39-05, Feb-Mar 2018. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/766354
  • Dataset
    Nitrogen and carbon fixation rates from bulk water samples from RV/Atlantic cruise AT39-05, Feb-Mar 2018
    (Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2020-05-04) Hutchins, David A. ; Webb, Eric A
    Nitrogen and carbon fixation rates from bulk water samples from RV/Atlantic cruise AT39-05, Feb-Mar 2018. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/766334
  • Dataset
    POC and PON from bulk seawater samples from RV/Atlantic cruise AT39-05, Feb-Mar 2018
    (Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu, 2020-05-04) Hutchins, David A. ; Webb, Eric A
    POC and PON from bulk seawater samples from RV/Atlantic cruise AT39-05, Feb-Mar 2018. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/766374
  • Article
    Co-occurrence of fe and P stress in natural populations of the marine diazotroph Trichodesmium
    (European Geosciences Union, 2020-05-12) Held, Noelle A. ; Webb, Eric A. ; McIlvin, Matthew R. ; Hutchins, David A. ; Cohen, Natalie R. ; Moran, Dawn M. ; Kunde, Korinna ; Lohan, Maeve C. ; Mahaffey, Claire ; Woodward, E. Malcolm S. ; Saito, Mak A.
    Trichodesmium is a globally important marine microbe that provides fixed nitrogen (N) to otherwise N-limited ecosystems. In nature, nitrogen fixation is likely regulated by iron or phosphate availability, but the extent and interaction of these controls are unclear. From metaproteomics analyses using established protein biomarkers for nutrient stress, we found that iron–phosphate co-stress is the norm rather than the exception for Trichodesmium colonies in the North Atlantic Ocean. Counterintuitively, the nitrogenase enzyme was more abundant under co-stress as opposed to single nutrient stress. This is consistent with the idea that Trichodesmium has a specific physiological state during nutrient co-stress. Organic nitrogen uptake was observed and occurred simultaneously with nitrogen fixation. The quantification of the phosphate ABC transporter PstA combined with a cellular model of nutrient uptake suggested that Trichodesmium is generally confronted by the biophysical limits of membrane space and diffusion rates for iron and phosphate acquisition in the field. Colony formation may benefit nutrient acquisition from particulate and organic sources, alleviating these pressures. The results highlight that to predict the behavior of Trichodesmium, both Fe and P stress must be evaluated simultaneously.
  • Article
    Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades
    (Springer, 2023-02-23) Webb, Eric A. ; Held, Noelle A. ; Zhao, Yiming ; Graham, Elaina D. ; Conover, Asa E. ; Semones, Jake ; Lee, Michael D. ; Feng, Yuanyuan ; Fu, Fei-Xue ; Saito, Mak A. ; Hutchins, David A.
    The colony-forming cyanobacteria Trichodesmium spp. are considered one of the most important nitrogen-fixing genera in the warm, low nutrient ocean. Despite this central biogeochemical role, many questions about their evolution, physiology, and trophic interactions remain unanswered. To address these questions, we describe Trichodesmium pangenomic potential via significantly improved genomic assemblies from two isolates and 15 new >50% complete Trichodesmium metagenome-assembled genomes from hand-picked, Trichodesmium colonies spanning the Atlantic Ocean. Phylogenomics identified ~four Nfixing clades of Trichodesmium across the transect, with T. thiebautii dominating the colony-specific reads. Pangenomic analyses showed that all T. thiebautii MAGs are enriched in COG defense mechanisms and encode a vertically inherited Type III-B Clustered Regularly Interspaced Short Palindromic Repeats and associated protein-based immunity system (CRISPR-Cas). Surprisingly, this CRISPR-Cas system was absent in all T. erythraeum genomes, vertically inherited by T. thiebautii, and correlated with increased signatures of horizontal gene transfer. Additionally, the system was expressed in metaproteomic and transcriptomic datasets and CRISPR spacer sequences with 100% identical hits to field-assembled, putative phage genome fragments were identified. While the currently CO-limited T. erythraeum is expected to be a 'winner' of anthropogenic climate change, their genomic dearth of known phage resistance mechanisms, compared to T. thiebautii, could put this outcome in question. Thus, the clear demarcation of T. thiebautii maintaining CRISPR-Cas systems, while T. erythraeum does not, identifies Trichodesmium as an ecologically important CRISPR-Cas model system, and highlights the need for more research on phage-Trichodesmium interactions.