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Ribalet, F.

Publications and source records attributed to Ribalet, F..

7 recordsLinked to original sources

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↗

A flexible Bayesian approach to estimating size-structured matrix population models

The rates of cell growth, division, and carbon loss of microbial populations are key parameters for understanding how organisms interact with their environment and how they contribute to the carbon cycle. However, the invasive nature of current analytical methods has hindered efforts to reliably quantify these parameters. In recent years, size-structured matrix population models (MPMs) have gained popularity for estimating rate parameters of microbial populations by mechanistically describing changes in microbial cell size distributions over time. And yet, the construction, analysis, and biological interpretation of these models are underdeveloped, as current implementations do not adequately constrain or assess the biological feasibility of parameter values, leading to inference which may provide a good fit to observed size distributions but does not necessarily reflect realistic physiological dynamics. Here we present a flexible Bayesian extension of size-structured MPMs for testing underlying assumptions describing the dynamics of a marine phytoplankton population over the day-night cycle. Our Bayesian framework takes prior scientific knowledge into account and generates biologically interpretable results. Using data from an exponentially growing laboratory culture of the cyanobacterium Prochlorococcus, we herein demonstrate the performance improvements of our approach over current models and isolate previously ignored biological processes, such as respiratory and exudative carbon losses, as critical parameters for the modeling of microbial population dynamics. The results demonstrate that this modeling framework can provide deeper insights into microbial population dynamics provided by flow-cytometry time-series data. Author summaryIdentifying the growth and population dynamics of marine microorganisms in their natural habitat is crucial to understanding the flow of carbon in the oceans but remains a grand challenge due to the invasive nature of current measurement methods. As time-series observations of population size structure have become more commonplace in aquatic environments, matrix population models (MPMs), which aim to mechanistically describe the change in size structure of these populations over time, have gained in popularity over the last decade. However, the underlying assumptions and behavior of MPMs have not been adequately scrutinized, and parameter values are difficult to interpret biologically, leading to inference that may not reflect plausible physiological dynamics. Here, we develop a Bayesian extension of the MPM framework to examine biological assumptions, improve interpretability of model output, and account for additional biological processes. We evaluated the performance of our models on a publicly available dataset of laboratory experiment time-series measurements of the cyanobacterium Prochlorococcus, Earths most abundant photosynthetic organisms, demonstrated the performance improvements of our approach over current models, and isolated previously ignored respiratory and exudative carbon losses as critical parameters for the modeling of microbial population dynamics.

microbiology↗

Diel population dynamics and mortality of Prochlorococcus in the North Pacific Subtropical Gyre

Photosynthesis fuels primary production at the base of marine food webs. Yet, in many surface ocean ecosystems, diel-driven primary production is tightly coupled to daily loss. This tight coupling raises the question: which top-down drivers predominate in maintaining persistently stable picocyanobacterial populations over longer time scales? Motivated by high-frequency surface water measurements taken in the North Pacific Subtropical Gyre (NPSG), we developed multitrophic models to investigate bottom-up and top-down mechanisms underlying the balanced control of Prochlorococcus populations. We find that incorporating photosynthetic growth with viral- and predator-induced mortality is sufficient to recapitulate daily oscillations of Prochlorococcus abundances with baseline community abundances. In doing so, we infer that grazers function as the primary top-down factor despite high standing viral particle densities while identifying the potential for light-dependent viral traits and non-canonical loss factors to shape the structure and function of marine microbial communities.

ecology↗

Nitrogen fixation in mesoscale eddies of the North Pacific Subtropical Gyre: patterns and mechanisms

1.Mesoscale eddies have been shown to support elevated dinitrogen (N2) fixation rates (NFRs) and abundances of N2-fixing microorganisms (diazotrophs), but the mechanisms underlying these observations are not well understood. We explored relationships among NFRs and cyanobacterial diazotroph abundances in eddy pairs of opposite polarity sampled in the North Pacific Subtropical Gyre and compared our observations to seasonal trends from the Hawaii Ocean Time-series (HOT) program. Consistent with previous reports, we found that NFRs were anomalously high for this region (up to 3.7-fold above previous monthly HOT observations) in the centers of the sampled anticyclones, coinciding with elevated abundances of Crocosphaera in the summertime. We then coupled our field-based observations, together with transcriptomic analyses of nutrient stress marker genes and ecological models, to evaluate potential mechanisms controlling diazotroph abundance and activity at the mesoscale. Specifically, we evaluated the role of biological (via estimates of growth and grazing rates) and physical controls on populations of Crocosphaera, Trichodesmium, and diatom symbionts. Our results suggest that increased Crocosphaera abundances associated with summertime anticyclones resulted from the alleviation of phosphate limitation, allowing cells to grow at rates exceeding grazing losses. In contrast, distributions of larger, buoyant taxa (Trichodesmium and diatom symbionts) appeared less affected by eddy-driven biological controls. Instead, they appeared driven by physical dynamics along frontal boundaries that separate cyclonic and anticyclonic eddies. Together, the interplay of eddy-specific changes in bottom-up control, top-down control, and the physical accumulation of cells likely explains the elevated diazotroph abundances and NFRs associated with anticyclones and eddy fronts.

ecology↗

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↗

A Kernel-Based Change Detection Method to Map Shifts in Phytoplankton Communities Measured by Flow Cytometry

O_LIAutomated, ship-board flow cytometers provide high-resolution maps of phytoplankton composition over large swaths of the worlds oceans. They therefore pave the way for understanding how environmental conditions shape community structure. Identification of community changes along a cruise transect commonly segments the data into distinct regions. However, existing segmentation methods are generally not applicable to flow cytometry data, as this data is recorded as "point cloud" data, with hundreds or thousands of particles measured during each time interval. Moreover, nonparametric segmentation methods that do not rely on prior knowledge of the number of species, are desirable to map community shifts. C_LIO_LIWe present CytoSegmenter, a kernel-based change-point estimation method for segmenting point cloud data that does not rely on parametric assumptions on the data distributions. Our method relies on a Hilbertian embedding of point clouds that allows us to work with point cloud data similarly to vectorial data. The change-point locations can be found using an efficient dynamic programming algorithm. The method can be used to automatically segment long series of underway flow cytometry data. C_LIO_LIThrough an analysis of 12 cruises, we demonstrate that CytoSegmenter allows us to locate abrupt changes in phytoplankton community structure. We show that the changes in community structure generally coincide with changes in the temperature and salinity of the ocean. We also illustrate how the main parameter of CytoSegmenter can be easily calibrated using limited auxiliary annotated data. C_LIO_LICytoSegmenter is publicly available and implemented in the programming language Python. The method is generally applicable for segmenting series of point cloud data from any domain. Moreover, it readily scales to thousands of point clouds, each containing thousands of points. In the context of underway flow cytometry data, it does not require prior clustering of particles to define taxa labels, eliminating a potential source of error. This represents an important advance in automating the analysis of large datasets now emerging in biological oceanography and other fields. It also allows for the approach to potentially be applied during research cruises. C_LI

ecology↗

Diel Oscillations of Particulate Metabolites Reflect Synchronized Microbial Activity in the North Pacific Subtropical Gyre

Light is the primary input of energy into the sunlit ocean, driving daily oscillations in metabolism of primary producers. The consequences of this solar forcing have implications for the whole microbial community, yet in situ measurements of metabolites, direct products of cellular activity, over the diel cycle are scarce. We evaluated community-level biochemical consequences of diel oscillations in the North Pacific Subtropical Gyre by quantifying 79 metabolites in particulate organic matter in surface waters every four hours over eight days. Total particulate metabolite concentration peaked at dusk, even when normalized to biomass estimates. The concentrations of 70% of individual metabolites exhibited 24-hour periodicity. Despite the diverse organisms that use them, primary metabolites involved in anabolic processes and redox maintenance had significant 24-hour periodicity. Osmolytes exhibited the largest diel oscillations, implying rapid turnover and metabolic roles beyond cell turgor maintenance. Metatranscriptome analysis revealed the taxa involved in production and consumption of some metabolites, including the osmolyte trehalose. This compound displayed the largest diel oscillations in abundance and was likely produced by the nitrogen-fixing cyanobacterium Crocosphaera for energy storage. These findings demonstrate that paired measurements of particulate metabolites and transcripts resolve strategies microbes use to manage daily energy and redox oscillations.

ecology↗