Allen
Andrew E.
Allen
Andrew E.
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ArticleMethionine 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.
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ArticleHydrothermal trace metal release and microbial metabolism in the northeastern Lau Basin of the South Pacific Ocean(European Geosciences Union, 2021-10-06) Cohen, Natalie R. ; Noble, Abigail E. ; Moran, Dawn M. ; McIlvin, Matthew R. ; Goepfert, Tyler J. ; Hawco, Nicholas J. ; German, Christopher R. ; Horner, Tristan J. ; Lamborg, Carl H. ; McCrow, John P. ; Allen, Andrew E. ; Saito, Mak A.Bioactive trace metals are critical micronutrients for marine microorganisms due to their role in mediating biological redox reactions, and complex biogeochemical processes control their distributions. Hydrothermal vents may represent an important source of metals to microorganisms, especially those inhabiting low-iron waters, such as in the southwest Pacific Ocean. Previous measurements of primordial 3He indicate a significant hydrothermal source originating in the northeastern (NE) Lau Basin, with the plume advecting into the southwest Pacific Ocean at 1500–2000 m depth (Lupton et al., 2004). Studies investigating the long-range transport of trace metals associated with such dispersing plumes are rare, and the biogeochemical impacts on local microbial physiology have not yet been described. Here we quantified dissolved metals and assessed microbial metaproteomes across a transect spanning the tropical and equatorial Pacific with a focus on the hydrothermally active NE Lau Basin and report elevated iron and manganese concentrations across 441 km of the southwest Pacific. The most intense signal was detected near the Mangatolo Triple Junction (MTJ) and Northeast Lau Spreading Center (NELSC), in close proximity to the previously reported 3He signature. Protein content in distal-plume-influenced seawater, which was high in metals, was overall similar to background locations, though key prokaryotic proteins involved in metal and organic uptake, protein degradation, and chemoautotrophy were abundant compared to deep waters outside of the distal plume. Our results demonstrate that trace metals derived from the NE Lau Basin are transported over appreciable distances into the southwest Pacific Ocean and that bioactive chemical resources released from submarine vent systems are utilized by surrounding deep-sea microbes, influencing both their physiology and their contributions to ocean biogeochemical cycling.
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ArticleColony formation in Phaeocystis antarctica : connecting molecular mechanisms with iron biogeochemistry(Copernicus Publications on behalf of the European Geosciences Union, 2018-08-21) Bender, Sara J. ; Moran, Dawn M. ; McIlvin, Matthew R. ; Zheng, Hong ; McCrow, John P. ; Badger, Jonathan ; DiTullio, Giacomo R. ; Allen, Andrew E. ; Saito, Mak A.Phaeocystis antarctica is an important phytoplankter of the Ross Sea where it dominates the early season bloom after sea ice retreat and is a major contributor to carbon export. The factors that influence Phaeocystis colony formation and the resultant Ross Sea bloom initiation have been of great scientific interest, yet there is little known about the underlying mechanisms responsible for these phenomena. Here, we present laboratory and field studies on Phaeocystis antarctica grown under multiple iron conditions using a coupled proteomic and transcriptomic approach. P. antarctica had a lower iron limitation threshold than a Ross Sea diatom Chaetoceros sp., and at increased iron nutrition (>120pM Fe') a shift from flagellate cells to a majority of colonial cells in P. antarctica was observed, implying a role for iron as a trigger for colony formation. Proteome analysis revealed an extensive and coordinated shift in proteome structure linked to iron availability and life cycle transitions with 327 and 436 proteins measured as significantly different between low and high iron in strains 1871 and 1374, respectively. The enzymes flavodoxin and plastocyanin that can functionally replace iron metalloenzymes were observed at low iron treatments consistent with cellular iron-sparing strategies, with plastocyanin having a larger dynamic range. The numerous isoforms of the putative iron-starvation-induced protein (ISIP) group (ISIP2A and ISIP3) had abundance patterns coinciding with that of either low or high iron (and coincident flagellate or the colonial cell types in strain 1871), implying that there may be specific iron acquisition systems for each life cycle type. The proteome analysis also revealed numerous structural proteins associated with each cell type: within flagellate cells actin and tubulin from flagella and haptonema structures as well as a suite of calcium-binding proteins with EF domains were observed. In the colony-dominated samples a variety of structural proteins were observed that are also often found in multicellular organisms including spondins, lectins, fibrillins, and glycoproteins with von Willebrand domains. A large number of proteins of unknown function were identified that became abundant at either high or low iron availability. These results were compared to the first metaproteomic analysis of a Ross Sea Phaeocystis bloom to connect the mechanistic information to the in situ ecology and biogeochemistry. Proteins associated with both flagellate and colonial cells were observed in the bloom sample consistent with the need for both cell types within a growing bloom. Bacterial iron storage and B12 biosynthesis proteins were also observed consistent with chemical synergies within the colony microbiome to cope with the biogeochemical conditions. Together these responses reveal a complex, highly coordinated effort by P. antarctica to regulate its phenotype at the molecular level in response to iron and provide a window into the biology, ecology, and biogeochemistry of this group.