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Article ; Online: Microbial population dynamics decouple growth response from environmental nutrient concentration.

Fink, Justus Wilhelm / Held, Noelle A / Manhart, Michael

Proceedings of the National Academy of Sciences of the United States of America

2023 Volume 120, Issue 2, Page(s) e2207295120

Abstract: How the growth rate of a microbial population responds to the environmental availability of chemical nutrients and other resources is a fundamental question in microbiology. Models of this response, such as the widely used Monod model, are generally ... ...

Abstract	How the growth rate of a microbial population responds to the environmental availability of chemical nutrients and other resources is a fundamental question in microbiology. Models of this response, such as the widely used Monod model, are generally characterized by a maximum growth rate and a half-saturation concentration of the resource. What values should we expect for these half-saturation concentrations, and how should they depend on the environmental concentration of the resource? We survey growth response data across a wide range of organisms and resources. We find that the half-saturation concentrations vary across orders of magnitude, even for the same organism and resource. To explain this variation, we develop an evolutionary model to show that demographic fluctuations (genetic drift) can constrain the adaptation of half-saturation concentrations. We find that this effect fundamentally differs depending on the type of population dynamics: Populations undergoing periodic bottlenecks of fixed size will adapt their half-saturation concentrations in proportion to the environmental resource concentrations, but populations undergoing periodic dilutions of fixed size will evolve half-saturation concentrations that are largely decoupled from the environmental concentrations. Our model not only provides testable predictions for laboratory evolution experiments, but it also reveals how an evolved half-saturation concentration may not reflect the organism's environment. In particular, this explains how organisms in resource-rich environments can still evolve fast growth at low resource concentrations. Altogether, our results demonstrate the critical role of population dynamics in shaping fundamental ecological traits.
MeSH term(s)	Biological Evolution ; Population Dynamics ; Acclimatization ; Adaptation, Physiological ; Nutrients
Language	English
Publishing date	2023-01-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2207295120
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Article ; Online: Spatial and Temporal Resolution of Cyanobacterial Bloom Chemistry Reveals an Open-Ocean

Via, Christopher W / Grauso, Laura / McManus, Kelly M / Kirk, Riley D / Kim, Andrew M / Webb, Eric A / Held, Noelle A / Saito, Mak A / Scarpato, Silvia / Zimba, Paul V / Moeller, Peter D R / Mangoni, Alfonso / Bertin, Matthew J

Environmental science & technology

2024

Abstract: While the ecological role ... ...

Abstract	While the ecological role that
Language	English
Publishing date	2024-05-17
Publishing country	United States
Document type	Journal Article
ISSN	1520-5851
ISSN (online)	1520-5851
DOI	10.1021/acs.est.3c10739
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Article ; Online: Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades.

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

ISME communications

2023 Volume 3, Issue 1, Page(s) 15

Abstract: 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 ... ...

Abstract	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 N
Language	English
Publishing date	2023-02-23
Publishing country	England
Document type	Journal Article
ISSN	2730-6151
ISSN (online)	2730-6151
DOI	10.1038/s43705-023-00214-y
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Article: Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria.

Held, Noelle A / McIlvin, Matthew R / Moran, Dawn M / Laub, Michael T / Saito, Mak A

mSystems

2019 Volume 4, Issue 1

Abstract: 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 ...

Abstract	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
Language	English
Publishing date	2019-02-05
Publishing country	United States
Document type	Journal Article
ISSN	2379-5077
ISSN	2379-5077
DOI	10.1128/mSystems.00317-18
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Article ; Online: Dynamic diel proteome and daytime nitrogenase activity supports buoyancy in the cyanobacterium Trichodesmium.

Held, Noelle A / Waterbury, John B / Webb, Eric A / Kellogg, Riss M / McIlvin, Matthew R / Jakuba, Michael / Valois, Frederica W / Moran, Dawn M / Sutherland, Kevin M / Saito, Mak A

Nature microbiology

2022 Volume 7, Issue 2, Page(s) 300–311

Abstract: Cyanobacteria of the genus Trichodesmium provide about 80 Tg of fixed nitrogen to the surface ocean per year and contribute to marine biogeochemistry, including the sequestration of carbon dioxide. Trichodesmium fixes nitrogen in the daylight, despite ... ...

Abstract	Cyanobacteria of the genus Trichodesmium provide about 80 Tg of fixed nitrogen to the surface ocean per year and contribute to marine biogeochemistry, including the sequestration of carbon dioxide. Trichodesmium fixes nitrogen in the daylight, despite the incompatibility of the nitrogenase enzyme with oxygen produced during photosynthesis. While the mechanisms protecting nitrogenase remain unclear, all proposed strategies require considerable resource investment. Here we identify a crucial benefit of daytime nitrogen fixation in Trichodesmium spp. that may counteract these costs. We analysed diel proteomes of cultured and field populations of Trichodesmium in comparison with the marine diazotroph Crocosphaera watsonii WH8501, which fixes nitrogen at night. Trichodesmium's proteome is extraordinarily dynamic and demonstrates simultaneous photosynthesis and nitrogen fixation, resulting in balanced particulate organic carbon and particulate organic nitrogen production. Unlike Crocosphaera, which produces large quantities of glycogen as an energy store for nitrogenase, proteomic evidence is consistent with the idea that Trichodesmium reduces the need to produce glycogen by supplying energy directly to nitrogenase via soluble ferredoxin charged by the photosynthesis protein PsaC. This minimizes ballast associated with glycogen, reducing cell density and decreasing sinking velocity, thus supporting Trichodesmium's niche as a buoyant, high-light-adapted colony forming cyanobacterium. To occupy its niche of simultaneous nitrogen fixation and photosynthesis, Trichodesmium appears to be a conspicuous consumer of iron, and has therefore developed unique iron-acquisition strategies, including the use of iron-rich dust. Particle capture by buoyant Trichodesmium colonies may increase the residence time and degradation of mineral iron in the euphotic zone. These findings describe how cellular biochemistry defines and reinforces the ecological and biogeochemical function of these keystone marine diazotrophs.
MeSH term(s)	Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Carbon Dioxide/metabolism ; Light ; Nitrogen/metabolism ; Nitrogen Fixation ; Nitrogenase/genetics ; Nitrogenase/metabolism ; Proteome ; Time Factors ; Trichodesmium/enzymology ; Trichodesmium/genetics ; Trichodesmium/physiology
Chemical Substances	Bacterial Proteins ; Proteome ; Carbon Dioxide (142M471B3J) ; Nitrogenase (EC 1.18.6.1) ; Nitrogen (N762921K75)
Language	English
Publishing date	2022-01-10
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	2058-5276
ISSN (online)	2058-5276
DOI	10.1038/s41564-021-01028-1
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Article ; Online: METATRYP v 2.0: Metaproteomic Least Common Ancestor Analysis for Taxonomic Inference Using Specialized Sequence Assemblies-Standalone Software and Web Servers for Marine Microorganisms and Coronaviruses.

Saunders, Jaclyn K / Gaylord, David A / Held, Noelle A / Symmonds, Nicholas / Dupont, Christopher L / Shepherd, Adam / Kinkade, Danie B / Saito, Mak A

Journal of proteome research

2020 Volume 19, Issue 11, Page(s) 4718–4729

Abstract: We present METATRYP version 2 software that identifies shared peptides across the predicted proteomes of organisms within environmental metaproteomics studies to enable accurate taxonomic attribution of peptides during protein inference. Improvements ... ...

Abstract	We present METATRYP version 2 software that identifies shared peptides across the predicted proteomes of organisms within environmental metaproteomics studies to enable accurate taxonomic attribution of peptides during protein inference. Improvements include ingestion of complex sequence assembly data categories (metagenomic and metatranscriptomic assemblies, single cell amplified genomes, and metagenome assembled genomes), prediction of the least common ancestor (LCA) for a peptide shared across multiple organisms, increased performance through updates to the backend architecture, and development of a web portal (https://metatryp.whoi.edu). Major expansion of the marine METATRYP database with predicted proteomes from environmental sequencing confirms a low occurrence of shared tryptic peptides among disparate marine microorganisms, implying tractability for targeted metaproteomics. METATRYP was designed to facilitate ocean metaproteomics and has been integrated into the Ocean Protein Portal (https://oceanproteinportal.org); however, it can be readily applied to other domains. We describe the rapid deployment of a coronavirus-specific web portal (https://metatryp-coronavirus.whoi.edu/) to aid in use of proteomics on coronavirus research during the ongoing pandemic. A coronavirus-focused METATRYP database identified potential SARS-CoV-2 peptide biomarkers and indicated very few shared tryptic peptides between SARS-CoV-2 and other disparate taxa analyzed, sharing <1% peptides with taxa outside of the betacoronavirus group, establishing that taxonomic specificity is achievable using tryptic peptide-based proteomic diagnostic approaches.
MeSH term(s)	Aquatic Organisms/genetics ; Bacterial Proteins/classification ; Bacterial Proteins/genetics ; Betacoronavirus/genetics ; COVID-19 ; Cluster Analysis ; Coronavirus/genetics ; Coronavirus Infections/virology ; Humans ; Metagenomics/methods ; Molecular Sequence Annotation ; Pandemics ; Peptides/classification ; Peptides/genetics ; Pneumonia, Viral/virology ; Proteome/classification ; Proteome/genetics ; SARS-CoV-2 ; Sequence Analysis, Protein ; Software ; Transcriptome/genetics ; Viral Proteins/classification ; Viral Proteins/genetics
Chemical Substances	Bacterial Proteins ; Peptides ; Proteome ; Viral Proteins
Keywords	covid19
Language	English
Publishing date	2020-09-23
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2078618-9
ISSN	1535-3907 ; 1535-3893
ISSN (online)	1535-3907
ISSN	1535-3893
DOI	10.1021/acs.jproteome.0c00385
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Article ; Online: Mechanisms and heterogeneity of in situ mineral processing by the marine nitrogen fixer Trichodesmium revealed by single-colony metaproteomics.

Held, Noelle A / Sutherland, Kevin M / Webb, Eric A / McIlvin, Matthew R / Cohen, Natalie R / Devaux, Alexander J / Hutchins, David A / Waterbury, John B / Hansel, Colleen M / Saito, Mak A

ISME communications

2021 Volume 1, Issue 1, Page(s) 35

Abstract: The keystone marine nitrogen fixer Trichodesmium thrives in high-dust environments. While laboratory investigations have observed that Trichodesmium colonies can access the essential nutrient iron from dust particles, less clear are the biochemical ... ...

Abstract	The keystone marine nitrogen fixer Trichodesmium thrives in high-dust environments. While laboratory investigations have observed that Trichodesmium colonies can access the essential nutrient iron from dust particles, less clear are the biochemical strategies underlying particle-colony interactions in nature. Here we demonstrate that Trichodesmium colonies engage with mineral particles in the wild with distinct molecular responses. We encountered particle-laden Trichodesmium colonies at a sampling location in the Southern Caribbean Sea; microscopy and synchrotron-based imaging then demonstrated heterogeneous associations with iron oxide and iron-silicate minerals. Metaproteomic analysis of individual colonies by a new low-biomass approach revealed responses in biogeochemically relevant proteins including photosynthesis proteins and metalloproteins containing iron, nickel, copper, and zinc. The iron-storage protein ferritin was particularly enriched implying accumulation of mineral-derived iron, and multiple iron acquisition pathways including Fe(II), Fe(III), and Fe-siderophore transporters were engaged. While the particles provided key trace metals such as iron and nickel, there was also evidence that Trichodesmium was altering its strategy to confront increased superoxide production and metal exposure. Chemotaxis regulators also responded to mineral presence suggesting involvement in particle entrainment. These molecular responses are fundamental to Trichodesmium's ecological success and global biogeochemical impact, and may contribute to the leaching of particulate trace metals with implications for global iron and carbon cycling.
Language	English
Publishing date	2021-07-13
Publishing country	England
Document type	Journal Article
ISSN	2730-6151
ISSN (online)	2730-6151
DOI	10.1038/s43705-021-00034-y
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Article: METATRYP v 2.0: Metaproteomic Least Common Ancestor Analysis for Taxonomic Inference Using Specialized Sequence Assemblies-Standalone Software and Web Servers for Marine Microorganisms and Coronaviruses

Saunders, Jaclyn K / Gaylord, David A / Held, Noelle A / Symmonds, Nicholas / Dupont, Christopher L / Shepherd, Adam / Kinkade, Danie B / Saito, Mak A

J Proteome Res

Abstract	We present METATRYP version 2 software that identifies shared peptides across the predicted proteomes of organisms within environmental metaproteomics studies to enable accurate taxonomic attribution of peptides during protein inference. Improvements include ingestion of complex sequence assembly data categories (metagenomic and metatranscriptomic assemblies, single cell amplified genomes, and metagenome assembled genomes), prediction of the least common ancestor (LCA) for a peptide shared across multiple organisms, increased performance through updates to the backend architecture, and development of a web portal (https://metatryp.whoi.edu). Major expansion of the marine METATRYP database with predicted proteomes from environmental sequencing confirms a low occurrence of shared tryptic peptides among disparate marine microorganisms, implying tractability for targeted metaproteomics. METATRYP was designed to facilitate ocean metaproteomics and has been integrated into the Ocean Protein Portal (https://oceanproteinportal.org); however, it can be readily applied to other domains. We describe the rapid deployment of a coronavirus-specific web portal (https://metatryp-coronavirus.whoi.edu/) to aid in use of proteomics on coronavirus research during the ongoing pandemic. A coronavirus-focused METATRYP database identified potential SARS-CoV-2 peptide biomarkers and indicated very few shared tryptic peptides between SARS-CoV-2 and other disparate taxa analyzed, sharing <1% peptides with taxa outside of the betacoronavirus group, establishing that taxonomic specificity is achievable using tryptic peptide-based proteomic diagnostic approaches.
Keywords	covid19
Publisher	WHO
Document type	Article
Note	WHO #Covidence: #748160
Database	COVID19

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Article ; Online: Development of an Ocean Protein Portal for Interactive Discovery and Education.

Saito, Mak A / Saunders, Jaclyn K / Chagnon, Michael / Gaylord, David A / Shepherd, Adam / Held, Noelle A / Dupont, Christopher / Symmonds, Nicholas / York, Amber / Charron, Matthew / Kinkade, Danie B

Journal of proteome research

2020 Volume 20, Issue 1, Page(s) 326–336

Abstract: Proteins are critical in catalyzing chemical reactions, forming key cellular structures, and in regulating cellular processes. Investigation of marine microbial proteins by metaproteomics methods enables the discovery of numerous aspects of microbial ... ...

Abstract	Proteins are critical in catalyzing chemical reactions, forming key cellular structures, and in regulating cellular processes. Investigation of marine microbial proteins by metaproteomics methods enables the discovery of numerous aspects of microbial biogeochemical processes. However, these datasets present big data challenges as they often involve many samples collected across broad geospatial and temporal scales, resulting in thousands of protein identifications, abundances, and corresponding annotation information. The Ocean Protein Portal (OPP) was created to enable data sharing and discovery among multiple scientific domains and serve both research and education functions. The portal focuses on three use case questions: "Where is my protein of interest?", "Who makes it?", and "How much is there?" and provides profile and section visualizations, real-time taxonomic analysis, and links to metadata, sequence analysis, and other external resources to enable connections to be made between biogeochemical and proteomics datasets.
MeSH term(s)	Information Dissemination ; Oceans and Seas ; Proteomics
Language	English
Publishing date	2020-12-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2078618-9
ISSN	1535-3907 ; 1535-3893
ISSN (online)	1535-3907
ISSN	1535-3893
DOI	10.1021/acs.jproteome.0c00382
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Article ; Online: Dinoflagellates alter their carbon and nutrient metabolic strategies across environmental gradients in the central Pacific Ocean.

Cohen, Natalie R / McIlvin, Matthew R / Moran, Dawn M / Held, Noelle A / Saunders, Jaclyn K / Hawco, Nicholas J / Brosnahan, Michael / DiTullio, Giacomo R / Lamborg, Carl / McCrow, John P / Dupont, Chris L / Allen, Andrew E / Saito, Mak A

Nature microbiology

2021 Volume 6, Issue 2, Page(s) 173–186

Abstract: Marine microeukaryotes play a fundamental role in biogeochemical cycling through the transfer of energy to higher trophic levels and vertical carbon transport. Despite their global importance, microeukaryote physiology, nutrient metabolism and ... ...

Abstract	Marine microeukaryotes play a fundamental role in biogeochemical cycling through the transfer of energy to higher trophic levels and vertical carbon transport. Despite their global importance, microeukaryote physiology, nutrient metabolism and contributions to carbon cycling across offshore ecosystems are poorly characterized. Here, we observed the prevalence of dinoflagellates along a 4,600-km meridional transect extending across the central Pacific Ocean, where oligotrophic gyres meet equatorial upwelling waters rich in macronutrients yet low in dissolved iron. A combined multi-omics and geochemical analysis provided a window into dinoflagellate metabolism across the transect, indicating a continuous taxonomic dinoflagellate community that shifted its functional transcriptome and proteome as it extended from the euphotic to the mesopelagic zone. In euphotic waters, multi-omics data suggested that a combination of trophic modes were utilized, while mesopelagic metabolism was marked by cytoskeletal investments and nutrient recycling. Rearrangement in nutrient metabolism was evident in response to variable nitrogen and iron regimes across the gradient, with no associated change in community assemblage. Total dinoflagellate proteins scaled with particulate carbon export, with both elevated in equatorial waters, suggesting a link between dinoflagellate abundance and total carbon flux. Dinoflagellates employ numerous metabolic strategies that enable broad occupation of central Pacific ecosystems and play a dual role in carbon transformation through both photosynthetic fixation in the euphotic zone and remineralization in the mesopelagic zone.
MeSH term(s)	Carbon Cycle ; Dinoflagellida/classification ; Dinoflagellida/metabolism ; Pacific Ocean ; Phylogeny ; Protozoan Proteins/metabolism ; Seawater/parasitology
Chemical Substances	Protozoan Proteins
Language	English
Publishing date	2021-01-04
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	2058-5276
ISSN (online)	2058-5276
DOI	10.1038/s41564-020-00814-7
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