ALBERT

Description: © The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biogeosciences 15 (2018): 4923-4942, doi:10.5194/bg-15-4923-2018.

Description: 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.

Description: Support for this study was provided by an Investigator grant to Mak A. Saito from the Gordon and Betty Moore Foundation (GBMF3782), National Science Foundation grants NSF-PLR 0732665, OCE-1435056, OCE-1220484, and ANT-1643684, the WHOI Coastal Ocean Institute, and a CINAR Postdoctoral Scholar Fellowship provided to Sara J. Bender through the Woods Hole Oceanographic Institution. Support was provided to Andrew E. Allen through NSF awards ANT-0732822, ANT-1043671, and OCE-1136477 and Gordon and Betty Moore Foundation grant GBMF3828. Additional support was provided to GRD through NSF award OPP-0338097.

Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 License. The definitive version was published in mSystems 4(1), (2019): 4:e00317-18, doi:10.1128/mSystems.00317-18.

Description: Two-component sensory (TCS) systems link microbial physiology to the environment and thus may play key roles in biogeochemical cycles. In this study, we surveyed the TCS systems of 328 diverse marine bacterial species. We identified lifestyle traits such as copiotrophy and diazotrophy that are associated with larger numbers of TCS system genes within the genome. We compared marine bacterial species with 1,152 reference bacterial species from a variety of habitats and found evidence of extra response regulators in marine genomes. Examining the location of TCS genes along the circular bacterial genome, we also found that marine bacteria have a large number of “orphan” genes, as well as many hybrid histidine kinases. The prevalence of “extra” response regulators, orphan genes, and hybrid TCS systems suggests that marine bacteria break with traditional understanding of how TCS systems operate. These trends suggest prevalent regulatory networking, which may allow coordinated physiological responses to multiple environmental signals and may represent a specific adaptation to the marine environment. We examine phylogenetic and lifestyle traits that influence the number and structure of two-component systems in the genome, finding, for example, that a lack of two-component systems is a hallmark of oligotrophy. Finally, in an effort to demonstrate the importance of TCS systems to marine biogeochemistry, we examined the distribution of Prochlorococcus/Synechococcus response regulator PMT9312_0717 in metaproteomes of the tropical South Pacific. We found that this protein’s abundance is related to phosphate concentrations, consistent with a putative role in phosphate regulation.

Description: We thank Joe Jennings at Oregon State University and Chris Dupont at the J. Craig Venter Institute for providing nutrient and metagenomic analyses, respectively, for the KM1128 METZYME research expedition. We also thank our anonymous reviewers for their thoughtful comments. This material is based on work supported by a National Science Foundation Graduate Research Fellowship under grant number 1122274 (N. A. Held). It was also supported by the Gordon and Betty Moore Foundation (grant number 3782 [M. Saito]) and by the National Science Foundation (grant numbers OCE-1657766, EarthCube 1639714, OCE-1658030, and OCE-1260233).

Description: © The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biogeosciences 14 (2017): 4637-4662, doi:10.5194/bg-14-4637-2017.

Description: The stoichiometry of biological components and their influence on dissolved distributions have long been of interest in the study of the oceans. Cobalt has the smallest oceanic inventory of inorganic micronutrients and hence is particularly vulnerable to influence by internal oceanic processes including euphotic zone uptake, remineralization, and scavenging. Here we observe not only large variations in dCo : P stoichiometry but also the acceleration of those dCo : P ratios in the upper water column in response to several environmental processes. The ecological stoichiometry of total dissolved cobalt (dCo) was examined using data from a US North Atlantic GEOTRACES transect and from a zonal South Atlantic GEOTRACES-compliant transect (GA03/3_e and GAc01) by Redfieldian analysis of its statistical relationships with the macronutrient phosphate. Trends in the dissolved cobalt to phosphate (dCo : P) stoichiometric relationships were evident in the basin-scale vertical structure of cobalt, with positive dCo : P slopes in the euphotic zone and negative slopes found in the ocean interior and in coastal environments. The euphotic positive slopes were often found to accelerate towards the surface and this was interpreted as being due to the combined influence of depleted phosphate, phosphorus-sparing (conserving) mechanisms, increased alkaline phosphatase metalloenzyme production (a zinc or perhaps cobalt enzyme), and biochemical substitution of Co for depleted Zn. Consistent with this, dissolved Zn (dZn) was found to be drawn down to only 2-fold more than dCo, despite being more than 18-fold more abundant in the ocean interior. Particulate cobalt concentrations increased in abundance from the base of the euphotic zone to become  ∼  10 % of the overall cobalt inventory in the upper euphotic zone with high stoichiometric values of  ∼  400 µmol Co mol−1 P. Metaproteomic results from the Bermuda Atlantic Time-series Study (BATS) station found cyanobacterial isoforms of the alkaline phosphatase enzyme to be prevalent in the upper water column, as well as a sulfolipid biosynthesis protein indicative of P sparing. The negative dCo : P relationships in the ocean interior became increasingly vertical with depth, and were consistent with the sum of scavenging and remineralization processes (as shown by their dCo : P vector sums). Attenuation of the remineralization with depth resulted in the increasingly vertical dCo : P relationships. Analysis of particulate Co with particulate Mn and particulate phosphate also showed positive linear relationships below the euphotic zone, consistent with the presence and increased relative influence of Mn oxide particles involved in scavenging. Visualization of dCo : P slopes across an ocean section revealed hotspots of scavenging and remineralization, such as at the hydrothermal vents and below the oxygen minimum zone (OMZ) region, respectively, while that of an estimate of Co* illustrated stoichiometrically depleted values in the mesopelagic and deep ocean due to scavenging. This study provides insights into the coupling between the dissolved and particulate phase that ultimately creates Redfield stoichiometric ratios, demonstrating that the coupling is not an instantaneous process and is influenced by the element inventory and rate of exchange between phases. Cobalt's small water column inventory and the influence of external factors on its biotic stoichiometry can erode its limited inertia and result in an acceleration of the dissolved stoichiometry towards that of the particulate phase in the upper euphotic zone. As human use of cobalt grows exponentially with widespread adoption of lithium ion batteries, there is a potential to affect the limited biogeochemical inertia of cobalt and its resultant ecology in the oceanic euphotic zone.

Description: This work was funded by the National Science Foundation as part of the US GEOTRACES North Atlantic Zonal Transect program under grants OCE-0928414 and OCE-1435056 (to Mak A. Saito), OCE-0928289 (to Benjamin S. Twining), OCE-0963026 (to Phoebe Lam) and support from the Gordon and Betty Moore Foundation (3782 to Mak A. Saito).