Bertrand Erin M.

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Erin M.

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  • Article
    Iron limitation of a springtime bacterial and phytoplankton community in the Ross Sea : implications for vitamin B12 nutrition
    (Frontiers Media, 2011-08-15) Bertrand, Erin M. ; Saito, Mak A. ; Lee, Peter A. ; Dunbar, Robert B. ; Sedwick, Peter N. ; DiTullio, Giacomo R.
    The Ross Sea is home to some of the largest phytoplankton blooms in the Southern Ocean. Primary production in this system has previously been shown to be iron limited in the summer and periodically iron and vitamin B12 colimited. In this study, we examined trace metal limitation of biological activity in the Ross Sea in the austral spring and considered possible implications for vitamin B12 nutrition. Bottle incubation experiments demonstrated that iron limited phytoplankton growth in the austral spring while B12, cobalt, and zinc did not. This is the first demonstration of iron limitation in a Phaeocystis antarctica-dominated, early season Ross Sea phytoplankton community. The lack of B12 limitation in this location is consistent with previous Ross Sea studies in the austral summer, wherein vitamin additions did not stimulate P. antarctica growth and B12 was limiting only when bacterial abundance was low. Bottle incubation experiments and a bacterial regrowth experiment also revealed that iron addition directly enhanced bacterial growth. B12 uptake measurements in natural water samples and in an iron fertilized bottle incubation demonstrated that bacteria serve not only as a source for vitamin B12, but also as a significant sink, and that iron additions enhanced B12 uptake rates in phytoplankton but not bacteria. Additionally, vitamin uptake rates did not become saturated upon the addition of up to 95 pM B12. A rapid B12 uptake rate was observed after 13 min, which then decreased to a slower constant uptake rate over the next 52 h. Results from this study highlight the importance of iron availability in limiting early season Ross Sea phytoplankton growth and suggest that rates of vitamin B12 production and consumption may be impacted by iron availability.
  • Article
    A seasonal study of dissolved cobalt in the Ross Sea, Antarctica : micronutrient behavior, absence of scavenging, and relationships with Zn, Cd, and P
    (Copernicus Publications on behalf of the European Geosciences Union, 2010-12-22) Saito, Mak A. ; Goepfert, Tyler J. ; Noble, Abigail E. ; Bertrand, Erin M. ; Sedwick, Peter N. ; DiTullio, Giacomo R.
    We report the distribution of cobalt (Co) in the Ross Sea polynya during austral summer 2005–2006 and the following austral spring 2006. The vertical distribution of total dissolved Co (dCo) was similar to soluble reactive phosphate (PO43−), with dCo and PO43− showing a significant correlation throughout the water column (r2 = 0.87, 164 samples). A strong seasonal signal for dCo was observed, with most spring samples having concentrations ranging from ~45–85 pM, whereas summer dCo values were depleted below these levels by biological activity. Surface transect data from the summer cruise revealed concentrations at the low range of this seasonal variability (~30 pM dCo), with concentrations as low as 20 pM observed in some regions where PO43− was depleted to ~0.1 μM. Both complexed Co, defined as the fraction of dCo bound by strong organic ligands, and labile Co, defined as the fraction of dCo not bound by these ligands, were typically observed in significant concentrations throughout the water column. This contrasts the depletion of labile Co observed in the euphotic zone of other ocean regions, suggesting a much higher bioavailability for Co in the Ross Sea. An ecological stoichiometry of 37.6 μmol Co:mol−1 PO43− calculated from dissolved concentrations was similar to values observed in the subarctic Pacific, but approximately tenfold lower than values in the Eastern Tropical Pacific and Equatorial Atlantic. The ecological stoichiometries for dissolved Co and Zn suggest a greater overall use of Zn relative to Co in the shallow waters of the Ross Sea, with a Co:PO43−/Zn:PO43− ratio of 1:17. Comparison of these observed stoichiometries with values estimated in culture studies suggests that Zn is a key micronutrient that likely influences phytoplankton diversity in the Ross Sea. In contrast, the observed ecological stoichiometries for Co were below values necessary for the growth of eukaryotic phytoplankton in laboratory culture experiments conducted in the absence of added zinc, implying the need for significant Zn nutrition in the Zn-Co cambialistic enzymes. The lack of an obvious kink in the dissolved Co:PO43− relationship was in contrast to Zn:PO43− and Cd:PO43− kinks previously observed in the Ross Sea. An excess uptake mechanism for kink formation is proposed as a major driver of Cd:PO43− kinks, where Zn and Cd uptake in excess of that needed for optimal growth occurs at the base of the euphotic zone, and no clear Co kink occurs because its abundances are too low for excess uptake. An unusual characteristic of Co geochemistry in the Ross Sea is an apparent lack of Co scavenging processes, as inferred from the absence of dCo removal below the euphotic zone. We hypothesize that this vertical distribution reflects a low rate of Co scavenging by Mn oxidizing bacteria, perhaps due to Mn scarcity, relative to the timescale of the annual deep winter mixing in the Ross Sea. Thus Co exhibits nutrient-like behavior in the Ross Sea, in contrast to its hybrid-type behavior in other ocean regions, with implications for the possibility of increased marine Co inventories and utility as a paleooceanographic proxy.
  • Thesis
    Insights into vitamin B12 production, acquisition, and use by marine microbes
    (Massachusetts Institute of Technology and Woods Hole Oceanographic Institution, 2012-02) Bertrand, Erin M.
    The distribution and magnitude of marine primary production helps determine the ocean's role in global carbon cycling. Constraining factors that impact this productivity and elucidating selective pressures that drive the composition of marine microbial communities are thus essential aspects of marine biogeochemistry. Vitamin B12, also known as cobalamin, is a cobalt containing organometallic micronutrient produced by some bacteria and archaea and required by many eukaryotic phytoplankton for methionine biosynthesis and regeneration. Although the potential for vitamin B12 availability to impact primary production and phytoplankton species composition has long been recognized, the lack of molecular-level tools for studying B12 production, use and acquisition has limited inquiry into the role of the vitamin in marine biogeochemical processes. This thesis describes the development of such tools and implements them for the study of B12 dynamics in an Antarctic shelf ecosystem. Nucleic acid probes for B12 biosynthesis genes were designed and used to identify a potentially dominant group of B12 producers in the Ross Sea. The activity of this group was then verified by mass spectrometry-based peptide measurements. Then, possible interconnections between iron and B12 dynamics in this region were identified using field-based bottle incubation experiments and vitamin uptake measurements, showing that iron availability may impact both B12 production and consumption. Changes in diatom proteomes induced by low B12 and low iron availability were then examined and used to identify a novel B12 acquisition protein, CBA 1, in diatoms. This represents the first identification of a B12 acquisition protein in eukaryotic phytoplankton. Transcripts encoding CBAl were detected in natural phytoplankton communities, confirming that B12 acquisition is an important part of phytoplankton molecular physiology. Selected reaction monitoring mass spectrometry was used to measure the abundance of CBA 1 and methionine synthase proteins in diatoms cultures, revealing distinct protein abundance patterns as a function ofB12 availability. These peptide measurements were implemented to quantify methionine synthase proteins in McMurdo Sound, revealing that there is both B12 utilization and starvation in natural diatom communities and that these peptide measurements hold promise for revealing the metabolic status of marine ecosystems with respect to vitamin B12.
  • Preprint
    Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics
    ( 2011-01) Gobler, Christopher J. ; Berry, Dianna L. ; Dyhrman, Sonya T. ; Wilhelm, Steven W. ; Salamov, Asaf ; Lobanov, Alexei V. ; Zhang, Yan ; Collier, Jackie L. ; Wurch, Louie L. ; Kustka, Adam B. ; Dill, Brian D. ; Shah, Manesh ; VerBerkmoes, Nathan C. ; Kuo, Alan J. ; Terry, Astrid ; Pangilinan, Jasmyn ; Lindquist, Erika A. ; Lucas, Susan ; Paulsen, Ian T. ; Hattenrath-Lehmann, Theresa K. ; Talmage, Stephanie C. ; Walker, Elyse A. ; Koch, Florian ; Burson, Amanda M. ; Marcoval, Maria Alejandra ; Tang, Ying-Zhong ; LeCleir, Gary R. ; Coyne, Kathryn J. ; Berg, Gry M. ; Bertrand, Erin M. ; Saito, Mak A. ; Gladyshev, Vadim N. ; Grigoriev, Igor V.
    Harmful algal blooms (HABs) cause significant economic and ecological damage worldwide. Despite considerable efforts, a comprehensive understanding of the factors that promote these blooms has been lacking because the biochemical pathways that facilitate their dominance relative to other phytoplankton within specific environments have not been identified. Here, biogeochemical measurements demonstrated that the harmful 43 Aureococcus anophagefferens outcompeted co-occurring phytoplankton in estuaries with elevated levels of dissolved organic matter and turbidity and low levels of dissolved inorganic nitrogen. We subsequently sequenced the first HAB genome (A. anophagefferens) and compared its gene complement to those of six competing phytoplankton species identified via metaproteomics. Using an ecogenomic approach, we specifically focused on the gene sets that may facilitate dominance within the environmental conditions present during blooms. A. anophagefferens possesses a larger genome (56 mbp) and more genes involved in light harvesting, organic carbon and nitrogen utilization, and encoding selenium- and metal-requiring enzymes than competing phytoplankton. Genes for the synthesis of microbial deterrents likely permit the proliferation of this species with reduced mortality losses during blooms. Collectively, these findings suggest that anthropogenic activities resulting in elevated levels of turbidity, organic matter, and metals have opened a niche within coastal ecosystems that ideally suits the unique genetic capacity of A. anophagefferens and thus has facilitated the proliferation of this and potentially other HABs.
  • Article
    Methionine synthase interreplacement in diatom cultures and communities : implications for the persistence of B12 use by eukaryotic phytoplankton
    (Association for the Sciences of Limnology and Oceanography, 2013-07) Bertrand, Erin M. ; Moran, Dawn M. ; McIlvin, Matthew R. ; Hoffman, Jeffrey M. ; Allen, Andrew E. ; Saito, Mak A.
    Three proteins related to vitamin B12 metabolism in diatoms were quantified via selected reaction monitoring mass spectrometry: B12-dependent and B12-independent methionine synthase (MetH, MetE) and a B12 acquisition protein (CBA1). B12-mediated interreplacement of MetE and MetH metalloenzymes was observed in Phaeodactylum tricornutum where MetH abundance was highest (0.06 fmol µg−1 protein) under high B12 and MetE abundance increased to 3.25 fmol µg−1 protein under low B12 availability. Maximal MetE abundance was 60-fold greater than MetH, consistent with the expected ∼ 50–100-fold larger turnover number for MetH. MetE expression resulted in 30-fold increase in nitrogen and 40-fold increase in zinc allocated to methionine synthase activity under low B12. CBA1 abundance was 6-fold higher under low-B12 conditions and increased upon B12 resupply to starved cultures. While biochemical pathways that supplant B12 requirements exist and are utilized by organisms such as land plants, B12 use persists in eukaryotic phytoplankton. This study suggests that retention of B12 utilization by phytoplankton results in resource conservation under conditions of high B12 availability. MetE and MetH abundances were also measured in diatom communities from McMurdo Sound, verifying that both these proteins are expressed in natural communities. These protein measurements are consistent with previous studies suggesting that B12 availability influences Antarctic primary productivity. This study illuminates controls on expression of B12-related proteins, quantitatively assesses the metabolic consequences of B12 deprivation, and demonstrates that mass spectrometry–based protein measurements yield insight into the functioning of marine microbial communities.
  • Article
    Proteome changes driven by phosphorus deficiency and recovery in the brown tide-forming alga Aureococcus anophagefferens
    (Public Library of Science, 2011-12-14) Wurch, Louie L. ; Bertrand, Erin M. ; Saito, Mak A. ; Van Mooy, Benjamin A. S. ; Dyhrman, Sonya T.
    Shotgun mass spectrometry was used to detect proteins in the harmful alga, Aureococcus anophagefferens, and monitor their relative abundance across nutrient replete (control), phosphate-deficient (−P) and −P refed with phosphate (P-refed) conditions. Spectral counting techniques identified differentially abundant proteins and demonstrated that under phosphate deficiency, A. anophagefferens increases proteins involved in both inorganic and organic phosphorus (P) scavenging, including a phosphate transporter, 5′-nucleotidase, and alkaline phosphatase. Additionally, an increase in abundance of a sulfolipid biosynthesis protein was detected in −P and P-refed conditions. Analysis of the polar membrane lipids showed that cellular concentrations of the sulfolipid sulphoquinovosyldiacylglycerol (SQDG) were nearly two-fold greater in the −P condition versus the control condition, while cellular phospholipids were approximately 8-fold less. Transcript and protein abundances were more tightly coupled for gene products involved in P metabolism compared to those involved in a range of other metabolic functions. Comparison of protein abundances between the −P and P-refed conditions identified differences in the timing of protein degradation and turnover. This suggests that culture studies examining nutrient starvation responses will be valuable in interpreting protein abundance patterns for cellular nutritional status and history in metaproteomic datasets.
  • Article
    The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response
    (Public Library of Science, 2012-03-29) Dyhrman, Sonya T. ; Jenkins, Bethany D. ; Rynearson, Tatiana A. ; Saito, Mak A. ; Mercier, Melissa L. ; Alexander, Harriet ; Whitney, LeAnn P. ; Drzewianowski, Andrea ; Bulygin, Vladimir V. ; Bertrand, Erin M. ; Wu, Zhijin ; Benitez-Nelson, Claudia R. ; Heithoff, Abigail
    Phosphorus (P) is a critical driver of phytoplankton growth and ecosystem function in the ocean. Diatoms are an abundant class of marine phytoplankton that are responsible for significant amounts of primary production. With the control they exert on the oceanic carbon cycle, there have been a number of studies focused on how diatoms respond to limiting macro and micronutrients such as iron and nitrogen. However, diatom physiological responses to P deficiency are poorly understood. Here, we couple deep sequencing of transcript tags and quantitative proteomics to analyze the diatom Thalassiosira pseudonana grown under P-replete and P-deficient conditions. A total of 318 transcripts were differentially regulated with a false discovery rate of <0.05, and a total of 136 proteins were differentially abundant (p<0.05). Significant changes in the abundance of transcripts and proteins were observed and coordinated for multiple biochemical pathways, including glycolysis and translation. Patterns in transcript and protein abundance were also linked to physiological changes in cellular P distributions, and enzyme activities. These data demonstrate that diatom P deficiency results in changes in cellular P allocation through polyphosphate production, increased P transport, a switch to utilization of dissolved organic P through increased production of metalloenzymes, and a remodeling of the cell surface through production of sulfolipids. Together, these findings reveal that T. pseudonana has evolved a sophisticated response to P deficiency involving multiple biochemical strategies that are likely critical to its ability to respond to variations in environmental P availability.