Biology subjects

Bundy, R. M.

Publications and source records attributed to Bundy, R. M..

7 recordsLinked to original sources

bioRxiv2026

Defining traits of low-light adapted Prochlorococcus inhabiting surface waters of the Equatorial Pacific Ocean

A diverse array of photosynthetic phytoplankton drives primary production in equatorial surface waters. Among these, the cyanobacterium Prochlorococcus is an important contributor to net primary production in these typically iron-limited, high-nutrient and low-chlorophyll (HNLC) regions. Here, we explore the diversity of these organisms, in part, through targeted enrichment of Prochlorococcus cells using field-based high-speed cell sorting techniques. We demonstrate that the genomes of Prochlorococcus belonging to the low-light adapted LLI clade, and isolated from the surface of the Equatorial Pacific Ocean, are depleted in functions related to the assimilation of urea, nitrite, and amino acids. These are the first examples of LLI Prochlorococcus that have lost the ability to use nitrite, a trait considered to be a core feature of this clade. All new equatorial cultures of LLI Prochlorococcus appear to use a distinct isoform of protoporphyrinogen IX oxidase (HemG), for the biosynthesis of a chlorophyll precursor, that does not require the use of iron-containing heme. In contrast, the heme-dependent HemJ isoform is typically used by Prochlorococcus found outside equatorial HNLC waters. Together, these findings suggest that low-light adapted Prochlorococcus in the equatorial ocean possess accessory gene content that reflects adaptation to the generally iron-limited but nitrogen-replete conditions of surface waters.

microbiology↗

bioRxiv2023

Microbial siderophore production is tightly coupled to iron in hydrothermal plumes

Hydrothermal vents have emerged as an important source of iron to seawater, yet only a subset of iron is soluble and persists long enough to be available for surface biological uptake. The longevity and solubility of iron in seawater is governed by strong organic ligands, like siderophores, that are produced by marine microorganisms and are a part of the oceans dissolved iron-binding ligand pool. These ligands have been hypothesized to aid in the persistence of dissolved iron in hydrothermal environments. To explore this hypothesis, we measured iron, iron-binding ligands, and siderophores from 11 geochemically distinct sites along a 1,700 km section of the Mid-Atlantic Ridge. Siderophores were found in hydrothermal plumes at all sites, with proximity to the vent playing an important role in dictating siderophore types and diversity. The notable presence of amphiphilic siderophores may point to microbial utilization of siderophores to access particulate hydrothermal iron, and the exchange of dissolved and particulate iron. The tight coupling between strong ligands and dissolved iron within neutrally buoyant plumes across six distinct hydrothermal environments, and the presence of dissolved siderophores with siderophore-producing microbial genera, suggests that biological production of siderophores exerts a key control on hydrothermal dissolved iron concentrations.

biochemistry↗

bioRxiv2022

Seasonal siderophore uptake and biosynthesis associated with carbon flux at Station ALOHA

The North Pacific subtropical gyre is a globally important contributor to carbon uptake and an oligotrophic ecosystem primarily limited by nitrogen. The microbial community is also seasonally exposed to low iron due to biological consumption and seasonally variable iron delivery. In this study, we examined changes in iron uptake rates, dissolved siderophore concentrations, and siderophore biosynthesis at Station ALOHA across time (2013-2016) and depth (surface to 500 m) to observe changes in iron acquisition and internal cycling by the microbial community. The genetic potential for siderophore biosynthesis was widespread throughout the upper water column, and biosynthetic gene clusters peaked in spring and summer along with siderophore concentrations, suggesting changes in nutrient delivery, primary production, and carbon export impact iron acquisition over the seasonal cycle. Dissolved iron turnover times, calculated from iron-amended experiments conducted using surface (15 m) and mesopelagic (300 m) waters, ranged from 9-252 days. The shortest average turnover times at both depths were associated with inorganic iron additions (14{+/-}9 days) and the longest with iron bound to strong siderophores (148{+/-}225 days). Uptake rates of siderophore-bound iron were faster in the mesopelagic waters than in the surface, leading to high Fe:C uptake ratios of heterotrophic bacteria in the upper mesopelagic. The rapid cycling and high demand for Fe at 300 m suggests differences in microbial metabolism and iron acquisition in the mesopelagic compared to surface waters. Together, changes in siderophore production and consumption over the seasonal cycle suggest organic carbon availability impacts iron cycling at Station ALOHA. Scientific Significance StatementMicrobial community production in the subtropical oligotrophic North Pacific is limited by macronutrients such as nitrogen. However, dissolved iron is another important micronutrient that has seasonal inputs from dust and passing eddies, keeping the availability of iron low and episodic. Little attention has been paid to the microbial strategies for dealing with low iron to support primary production in the oligotrophic ocean, or how limited iron availability impacts the processing of sinking particulate organic carbon in this region. In this study, we explore iron cycling including siderophore production and uptake by the microbial community throughout the water column at Station ALOHA to examine how the microbial community adapts and responds to changing iron and carbon availability on seasonal timescales.

bioinformatics↗

bioRxiv2022

Siderophore production and utilization by microbes in the North Pacific Ocean

Siderophores are strong iron-binding molecules produced and utilized by microbes to acquire the limiting nutrient iron (Fe) from their surroundings. Despite their importance as a component of the iron-binding ligand pool in seawater, data on the distribution of siderophores and the microbes that use them are limited. Here we measured the concentrations and types of dissolved siderophores during two cruises in April 2016 and June 2017 that transited from the iron-replete, low-macronutrient North Pacific Subtropical Gyre (NPSG) through the North Pacific Transition Zone (NPTZ) to the iron-deplete, high-macronutrient North Pacific Subarctic Frontal Zone (SAFZ). Surface siderophore concentrations in 2017 were higher in the NPTZ (4.0 - 13.9 pM) than the SAFZ (1.2 - 5.1 pM), which may be partly attributed to stimulated siderophore production by environmental factors such as dust-derived iron concentrations (up to 0.51 nM). Multiple types of siderophores were identified on both cruises, including ferrioxamines, amphibactins and iron-free forms of photoreactive siderophores, which suggest active production and use of diverse siderophores across latitude and depth. Additionally, the widespread genetic potential for siderophore biosynthesis and uptake across latitude and the variability in the taxonomic composition of bacterial communities that transcribe putative ferrioxamine, amphibactin and salmochelin transporter genes at different latitudes suggest that particular microbes actively produce and use siderophores, altering siderophore distributions and the bioavailability of iron across the North Pacific.

ecology↗

bioRxiv2021

Siderophores as an iron source for Prochlorococcus in deep chlorophyll maximum layers of the oligotrophic ocean

Prochlorococcus is one of the most abundant photosynthesizing organisms in the oligotrophic oceans. Gene content variation among Prochlorococcus populations in separate ocean basins often mirrors the selective pressures imposed by the regions distinct biogeochemistry. By pairing genomic datasets with trace metal concentrations from across the global ocean, we show that the genomic capacity for siderophore-mediated iron uptake is widespread in low-light adapted Prochlorococcus populations from iron-depleted regions of the oligotrophic Pacific and S. Atlantic oceans: Prochlorococcus siderophore consumers were absent in the N. Atlantic ocean (higher iron flux) but constituted up to half of all Prochlorococcus genomes from metagenomes in the N. Pacific (lower iron flux). Prochlorococcus siderophore consumers, like many other bacteria with this trait, also lack siderophore biosynthesis genes indicating that they scavenge exogenous siderophores from seawater. Statistical modeling suggests that the capacity for siderophore uptake is endemic to remote ocean regions where atmospheric iron fluxes are the smallest, particularly at deep chlorophyll maximum and primary nitrite maximum layers. We argue that abundant siderophore consumers at these two common oceanographic features could be a symptom of wider community iron stress, consistent with prior hypotheses. Our results provide a clear example of iron as a selective force driving the evolution of Prochlorococcus.

ecology↗

bioRxiv2021

Diverse arsenic-containing lipids in the surface ocean

Arsenic is present at nanomolar levels throughout the surface ocean, and microbes assimilate this toxic element due to its similarity to inorganic phosphorus. Although the concentration and characterization of dissolved arsenic has been a focus of ocean studies, the size of the particulate arsenic pool and its partitioning into organic molecules within the microbial community is not known. We measured the particulate pool of arsenic in five surface samples from the open ocean and determined the contribution of arsenic-containing lipids to this pool. Here we show that the accumulation of arsenic into lipids is a widespread phenomenon in the surface ocean. Particulate arsenic concentrations were 15 to 42 pmol L-1 with 7-20% of the particulate arsenic pool in the form of arsenolipids. We characterized these arsenolipids and found that arsenosugar phospholipids dominated the arsenolipid pools in our samples with a minor component of arsenohydrocarbons and other unidentified lipids. A significant portion of the arsenosugar phospholipids (up to 35%) were present as previously undescribed mixed acyl ether lipids, suggesting a bacterial source. Scientific significance statementMarine microbes experience constant exposure to the toxic element arsenic. However, there are no baseline measurements of how much arsenic accumulates in microbial communities nor do we know the full spectrum of arsenic containing biomolecules produced in marine systems. In culture-based studies there is strong evidence that phytoplankton synthesize arsenic-containing lipids, but these lipids have not been observed in natural communities of marine microbes. Here we make measurements of bulk particulate arsenic at five sites in the surface open ocean and show that a significant portion of this particulate arsenic is present as complex arsenic-containing lipids. We characterize this arsenolipid pool chemically and quantitatively to show a variety of chemically distinct and quantitatively significant lipids that expand our understanding of marine arsenic biogeochemistry. Data availability statementMass spectrometry data and its associated metadata will be available on Dryad with publication. Scripts for data processing and figure generation found on github at https://github.com/kheal/particulate_As_data_analysis.

ecology↗

bioRxiv2020

Marine community metabolomes carry fingerprints of phytoplankton community composition

Phytoplankton transform inorganic carbon into thousands of biomolecules that represent an important pool of fixed carbon, nitrogen, and sulfur in the surface ocean. Metabolite production differs between phytoplankton, and the flux of these molecules through the microbial food web depends on compound-specific bioavailability to members of a wider microbial community. Yet relatively little is known about the diversity or concentration of metabolites within marine plankton. Here we compare 313 polar metabolites in 21 cultured phytoplankton species and in natural planktonic communities across environmental gradients to show that bulk community metabolomes reflect chemical composition of the phytoplankton community. We also show that groups of compounds have similar patterns across space and taxonomy suggesting that the concentrations of these compounds in the environment are controlled by similar sources and sinks. We quantify several compounds in the surface ocean that represent substantial understudied pools of labile carbon. For example, the N-containing metabolite homarine was up to 3% of particulate carbon and is produced in high concentrations by cultured Synechococcus, and S-containing gonyol accumulated up to 2.5 nM in surface particles and likely originates from dinoflagellates. Our results show that phytoplankton composition directly shapes the carbon composition of the surface ocean. Our findings suggest that in order to access these pools of bioavailable carbon, the wider microbial community must be adapted to phytoplankton community composition. IMPORTANCEMicroscopic phytoplankton transform 100 million tons of inorganic carbon into thousands of different organic compounds each day. The structure of each chemical is critical to its biological and ecosystem function, yet, the diversity of biomolecules produced by marine microbial communities remained mainly unexplored, especially small polar molecules which are often considered the currency of the microbial loop. Here we explore the abundance and diversity of small biomolecules in planktonic communities across ecological gradients in the North Pacific and within 21 cultured phytoplankton species. Our work demonstrates that phytoplankton diversity is an important determinant of the chemical composition of the highly bioavailable pool of organic carbon in the ocean, and we highlight understudied yet abundant compounds in both the environment and cultured organisms. These findings add to understanding of how the chemical makeup of phytoplankton shapes marine microbial communities where the ability to sense and use biomolecules depends on the chemical structure.

ecology↗