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  • 1
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    Protein regulation in Trichodesmium and other marine bacteria: observational and interpretive biomarkers of biogeochemical processes (2020)
    Massachusetts Institute of Technology and Woods Hole Oceanographic Institution
    Details
    Publication Date: 2022-05-26
    Description: Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Chemical Oceanography and Microbial Biogeochemistry at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution February 2020.
    Description: Marine microbes play key roles in global biogeochemistry by mediating chemical transformations and linking nutrient cycles to one another. A major goal in oceanography is to predict the activity of marine microbes across disparate ocean ecosystems. Towards this end, molecular biomarkers are important tools in chemical oceanography because they allow for both the observation and interpretation of microbial behavior. In this thesis, I use molecular biomarkers to develop a holistic, systems biology approach to the study of marine microbes. I begin by identifying unique patterns in the biochemical sensory systems of marine bacteria and suggest that these represent a specific adaptation to the marine environment. Building from this, I focus on the prevalent marine nitrogen fixer Trichodesmium, whose activity affects global nitrogen, carbon, phosphorus, and trace metal cycles. A metaproteomic survey of Trichodesmium populations identified simultaneous iron and phosphate co-stress throughout the tropical and subtropical oceans, demonstrating that this is caused by the biophysical limits of membrane space and nutrient diffusion. Tackling the problem at a smaller scale, I investigated the metaproteomes of individual Trichodesmium colonies captured from a single field site, and identified significant variability related to iron acquisition from mineral particles. Next, I investigated diel proteomes of cultured Trichodesmium erythraeum sp. IMS101 to highlight its physiological complexity and understand how and why nitrogen fixation occurs in the day, despite the incompatibly of the nitrogenase enzyme with oxygen produced in photosynthesis. This thesis develops a fundamental understanding of how Trichodesmium and other organisms affect, and are affected by, their surroundings. It indicates that a reductionist approach in which environmental drivers are considered independently may not capture the full complexity of microbechemistry interactions. Future work can focus on benchmarking and calibration of the protein biomarkers identified here, as well as continued connection of systems biology frameworks to the study of ocean chemistry.
    Description: This work was supported by an MIT Walter A. Rosenblith Presidential Fellowship and a National Science Foundation Graduate Research Program Fellowship under grant number 1122274 [N.Held]. This work was also supported by the WHOI Ocean Ventures fund [N.Held], Gordon and Betty Moore Foundation grant number 3782 [M.Saito], National Science Foundation grant numbers OCE-1657766 [M.Saito], EarthCube-1639714 [M.Saito], OCE-1658030 [M.Saito], and OCE-1260233 [M.Saito], and funding from the UK Natural Environment Research Council (NERC) under grants awarded to C.M. (NE/N001079/1) and M.L. (NE/N001125/1). This thesis was completed during a writing residency at the Turkeyland Cove Foundation.
    Repository Name: Woods Hole Open Access Server
    Type: Thesis
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  • 2
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    Unique patterns and biogeochemical relevance of two-component sensing in marine bacteria. (2019)
    American Society for Microbiology Journals
    Details
    Publication Date: 2022-10-26
    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).
    Keywords: Biogeochemistry ; Cell signaling ; Gene regulation ; Marine microbiology ; Proteomics ; Regulatory network ; Two-component system
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 3
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    Co-occurrence of fe and P stress in natural populations of the marine diazotroph Trichodesmium (2020)
    European Geosciences Union
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Held, N. A., Webb, E. A., McIlvin, M. M., Hutchins, D. A., Cohen, N. R., Moran, D. M., Kunde, K., Lohan, M. C., Mahaffey, C., Woodward, E. M. S., & Saito, M. A. Co-occurrence of fe and P stress in natural populations of the marine diazotroph Trichodesmium. Biogeosciences, 17(9), (2020): 2537-2551, doi:10.5194/bg-17-2537-2020.
    Description: 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.
    Description: This research has been supported by the National Science Foundation (Division of Graduate Education (grant nos. 1122274), Division of Ocean Sciences (grant nos. 1657755, 1657757, and 1851222), Directorate for Geosciences (grant no. 1639714)), the Gordon and Betty Moore Foundation (grant no. 3782), and the Natural Environment Research Council (NERC) (grant nos. NE/N001079/1 and NE/N001125/1).
    Repository Name: Woods Hole Open Access Server
    Type: Article
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