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Durham, B.

Publications and source records attributed to Durham, B..

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Picophytoplankton Implicated in Productivity and Biogeochemistry in the North Pacific Transition Zone

Marine phytoplankton are central to global seascapes, acting as key conduits in element cycling and oceanic food webs. Phytoplankton cell size spans several orders of magnitude (0.2 to >200 {micro}m) and is an important trait that governs metabolism. Yet, the vast taxonomic diversity within phytoplankton size classes makes it challenging to link specific taxa to bulk community changes in productivity and elemental stoichiometry. To explore phytoplankton biogeography and biogeochemical roles in field populations, we analyzed three years of 16S and 18S rRNA gene amplicon sequencing variant (ASV) data alongside biochemical measurements across the dynamic latitudinal gradient of the North Pacific Transition Zone. We (1) identified picophytoplankton community members associated with patterns in net community production (NCP), particulate organic carbon (POC), and particulate organic nitrogen (PON), and (2) uncovered co-occurring species that may influence their growth and abundance. Multivariate linear mixed modeling revealed that occurrence of chlorophytes explained 22.6% of NCP values, followed by stramenopiles and cyanobacteria. In contrast, POC and PON spatial patterns were best explained by chlorophyte and dinoflagellate spatial patterns. Weighted co-expression network analysis further showed NCP, POC, and PON correlations with a subset of [~]40 ASVs belonging to chlorophytes, cyanobacteria, stramenopiles, haptophytes, and dinoflagellates that range in trophic strategy. Association network inference recapitulated these findings and revealed additional co-occurring phytoplankton, grazers, and heterotrophic bacteria. Together, our integrated computational analyses identified key picophytoplankton and co-occurring mixotrophs as major contributors to shaping regional biogeochemical dynamics in the North Pacific Ocean. ImportancePhytoplankton mediate key biogeochemical processes in dynamic oceanic transition zones. Yet, their vast cell size range and taxonomic diversity makes it challenging to link specific taxa to bulk community changes in productivity and elemental stoichiometry. By integrating molecular and biogeochemical measurements from the North Pacific Transition Zone using combined network and multivariate modeling, we identified specific picophytoplankton strongly linked to community production and organic nutrients levels. These picophytoplankton included specific members of cyanobacteria, pelagophytes, haptophytes, and chlorophytes, and formed tight associations with several nano- and pico-sized protistan mixotrophs highlighting how top-down interactions and microbial consortia shape community structure and elemental fluxes. Our work establishes key microbial players that may control fundamental ecosystem processes like carbon and nitrogen cycling and offers a computational framework to track and identify "microbial neighborhoods" that underpin biogeochemical features of an ecosystem.

microbiology↗

The dynamic trophic architecture of open-ocean protist communities revealed through machine- guided metatranscriptomics

Intricate networks of single-celled eukaryotes (protists) dominate carbon flow in the ocean. Their growth, demise, and interactions with other microorganisms drive the fluxes of biogeochemical elements through marine ecosystems. Mixotrophic protists are capable of both photosynthesis and ingestion of prey and are dominant components of open-ocean planktonic communities. Yet, the role of mixotrophs in elemental cycling is obscured by their capacity to act as primary producers or heterotrophic consumers depending on factors that remain largely uncharacterized. Here we introduce a machine learning model that can predict the in situ nutritional mode of aquatic protists based on their patterns of gene expression. This approach leverages a public collection of protist transcriptomes as a training set to identify a subset of gene families whose transcriptional profiles predict trophic status. We applied our model to nearly 100 metatranscriptomes obtained during two oceanographic cruises in the North Pacific and found community-level and population-specific evidence that abundant open-ocean mixotrophic populations shift their predominant mode of nutrient and carbon acquisition in response to natural gradients in nutrient supply and sea surface temperature. In addition, metatranscriptomic data from ship-board incubation experiments revealed that abundant mixotrophic prymnesiophytes from the oligotrophic North Pacific subtropical gyre rapidly remodelled their transcriptome to enhance photosynthesis when supplied with limiting nutrients. Coupling the technique introduced here with experiments designed to reveal the mechanisms driving mixotroph physiology is a promising approach for understanding the ecology of mixotrophic populations in the natural environment. Significance statementMixotrophy is a ubiquitous nutritional strategy in marine ecosystems. Although our understanding of the distribution and abundance of mixotrophic plankton has improved significantly, the functional roles of mixotrophs are difficult to pinpoint, as mixotroph nutritional strategies are flexible and form a continuum between heterotrophy and phototrophy. We employ a machine learning-driven metatranscriptomic technique to assess the nutritional strategies of abundant planktonic populations in situ and demonstrate that mixotrophic populations play varying functional roles along physico-chemical gradients in the North Pacific Ocean, revealing a degree of physiological plasticity unique to aquatic mixotrophs. Our results highlight mechanisms that may dictate the flow of biogeochemical elements and the ecology of the North Pacific Ocean, one of the largest biogeographical provinces on Earth.

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↗

Impaired hematopoiesis and leukemia development in mice with a \"knock-in\" allele of U2af1(S34F)

Mutations affecting the spliceosomal protein U2AF1 are commonly found in myelodysplastic syndromes (MDS) and secondary acute myeloid leukemia (sAML). We have generated mice that carry Cre-dependent \"knock-in\" alleles of U2af1(S34F), the murine version of the most common mutant allele of U2AF1 encountered in human cancers. Cre-mediated recombination in murine hematopoietic lineages caused changes in RNA splicing, as well as multilineage cytopenia, macrocytic anemia, decreased hematopoietic stem and progenitor cells, low-grade dysplasias, and impaired transplantability, but without lifespan shortening or leukemia development. In an attempt to identify U2af1(S34F)-cooperating changes that promote leukemogenesis, we combined U2af1(S34F) with Runx1 deficiency in mice and further treated the mice with a mutagen, N-Ethyl-N-Nitrosourea (ENU). Overall, three of sixteen ENU-treated compound transgenic mice developed AML. However, AML did not arise in mice with other genotypes or without ENU treatment. Sequencing DNA from the three AMLs revealed somatic mutations homologous to those considered to be drivers of human AML, including predicted loss-or gain-of-function mutations in Tet2, Gata2, Idh1, and Ikzfl. However, the engineered U2af1(S34F) missense mutation reverted to wild type (WT) in two of the three AML cases, implying that U2af1(S34F) is dispensable, or even selected against, once leukemia is established.\n\nSIGNIFICANCE STATEMENTSomatic mutations in four splicing factor genes (U2AF1, SRSF2, SF3B1, and ZRSR2) are found in MDS and MDS-related AML, blood cancers with few effective treatment options. However, the pathophysiological effects of these mutations remain poorly characterized, in part due to the paucity of disease-relevant models. Here, we report the establishment of mouse models to study the most common U2AF1 mutation, U2af1(S34F). Production of the mutant protein specifically in the murine hematopoietic compartment disrupts hematopoiesis in ways resembling human MDS. We further identified deletion of the Runx1 gene and other known oncogenic mutations as changes that might collaborate with U2af1(S34F) to give rise to frank AML in mice.

cancer biology↗