Held
Noelle A.
Held
Noelle A.
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ThesisProtein regulation in Trichodesmium and other marine bacteria: observational and interpretive biomarkers of biogeochemical processes(Massachusetts Institute of Technology and Woods Hole Oceanographic Institution, 2020-02) Held, Noelle A.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.
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ArticleCo-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.
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ArticleImportance 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.
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ArticleUnique patterns and biogeochemical relevance of two-component sensing in marine bacteria.(American Society for Microbiology Journals, 2019-01-11) Held, Noelle A. ; McIlvin, Matthew R. ; Moran, Dawn M. ; Laub, Michael T. ; Saito, Mak A.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.