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Van Mooy, B. A. S.

Publications and source records attributed to Van Mooy, B. A. S..

7 recordsLinked to original sources

RNA virus-mediated metabolic reprogramming in a bloom-forming, marine diatom

Diatoms are a widespread group of phytoplankton that disproportionately influence the global carbon cycle through substantial contributions to primary production and carbon export in the ocean. Marine viruses are major drivers of host metabolic reprogramming and mortality and it is increasingly clear that RNA viruses, which primarily infect eukaryotes, are abundant and distributed throughout the global ocean. Using an integrated, multi-omics approach, we characterized the molecular and metabolic response of the model, bloom-forming, centric diatom Chaetoceros tenuissimus to RNA virus infection. Time-resolved transcriptomics revealed coordinated, differential regulation of more than a third of host genes prior to host lysis, eliciting a cascade of metabolic responses that included early shifts in sulfur and lipid metabolism, induction of nitrogen assimilation pathways, and late-stage activation of stress, signaling and death-related genes. Lipidomics revealed substantial cellular enrichment of phosphatidylethanolamine, ceramide and triacylglycerol during RNA virus infection, as well as an infection-specific shift in fatty acid composition. Collectively, these findings provide insight into the intracellular requirements for RNA virus replication and illustrate a fundamental shift in resource partitioning in infected diatoms, advancing our understanding of how RNA virus infection transforms diatom host metabolic function and downstream ecosystem dynamics.

microbiology↗

Exploring the Phaeosphere: characterizing the microbiomes of Phaeocystis antarctica colonies from the coastal Southern Ocean and laboratory culture

Interactions between phytoplankton and bacteria play critical roles in shaping marine ecosystems. However, the intricate relationships within these communities--particularly in extreme and rapidly changing environments like the coastal Southern Ocean--remain poorly understood. Here, we apply targeted methods to directly characterize the microbiomes of individual colonies of Phaeocystis antarctica, a keystone phytoplankton species in the Southern Ocean, for the first time. We show that colony microbiomes are consistent in distinct geographic locations at approximately the same time, but shift significantly after a year of laboratory culture. The bacterial orders Alteromonadales, Oceanospirillales, and Sphingomonadales dominated the microbiomes of all field-collected colonies, whereas Caulobacterales, Cellvibrionales, and Rhodobacterales dominated colony microbiomes after culturing. Notably, the most abundant genera in field-collected colony microbiomes, the psychrophiles Paraglaciecola and Colwellia, were lost in culture. The shift in microbiome structure emphasizes the importance of field-based studies to capture the complexity of microbial interactions, especially for species from polar environments that are difficult to replicate in laboratory conditions. Furthermore, the relative abundances of bacterial taxa comprising the majority of field-collected colony microbiomes--e.g., Paraglaciecola sp. (Alteromonadales) and Nitrincolaceae (Oceanospirillales)--were strongly associated with Phaeocystis abundance in surface waters, highlighting their potential roles in bloom dynamics and carbon cycling. This research provides valuable insights into the ecological significance of prokaryotic interactions with a key phytoplankton species and underscores the necessity of considering these dynamics in the context of climate-driven shifts in marine ecosystems.

microbiology↗

Microbial metabolic specificity controls pelagic lipid export efficiency

Lipids comprise more than 20% of sinking organic matter in the ocean and play a crucial role in the carbon cycle. Despite this, our understanding of the processes that control lipid degradation is limited. Here we combined nano-lipidomics and imaging to study the bacterial degradation of diverse algal lipid droplets. Bacteria isolated from natural marine particles exhibited distinct dietary preferences, ranging from selective to promiscuous degraders. Dietary preference was associated with a distinct set of lipid degradation genes rather than with taxonomic origin. The top degrader, Pseudomonas zhaodongensis, rapidly consumed triacylglycerols (TAGs) from lipid extracts while promoting colonization of kin by chemotaxis toward glycerol, the TAG degradation product. Using synthetic communities composed of isolates with distinct dietary preferences, we demonstrated that lipid degradation is modulated by microbial interactions. A particle export model incorporating these dynamics suggests that metabolic specialization and community dynamics influences lipid transport efficiency in the oceans mesopelagic zone.

ecology↗

Novel isolates expand the physiological diversity of Prochlorococcus and illuminate its macroevolution

Prochlorococcus is a diverse picocyanobacterial genus and the most abundant phototroph on Earth. Its photosynthetic diversity divides it into high- or low-light adapted groups representing broad phylogenetic grades - each composed of several monophyletic clades. Here we physiologically characterize four new Prochlorococcus strains isolated from below the deep chlorophyll maximum in the North Pacific Ocean and combine this information with genomic and evolutionary analyses. The isolates belong to deeply-branching low-light adapted clades that have no other cultivated representatives and display some unusual characteristics. For example, despite its otherwise low-light adapted physiological characteristics, strain MIT1223 has low chl b2 content similar to high-light adapted strains. Isolate genomes revealed that each strain contains a unique arsenal of pigment biosynthesis and binding alleles that have been horizontally acquired, contributing to the observed physiological diversity. Comparative genomic analysis of all picocyanobacteria reveals that Pcb, the major pigment carrying protein in Prochlorococcus, greatly increased in copy number and diversity per genome along a branch that coincides with the loss of facultative particle attachment. Collectively, these observations add support to the current macroevolutionary model of picocyanobacteria, where niche constructing radiations allowed ancestral lineages to transition from a particle-attached to planktonic lifestyle and broadly colonize the water column, followed by adaptive radiations near the surface that pushed ancestral lineages deeper in the euphotic zone resulting in modern depth-abundance profiles. Originality-Significance StatementThe marine cyanobacterium, Prochlorococcus, is among the Earths most abundant organisms, and much of its genetic and physiological diversity remains uncharacterized. While field studies help reveal the scope of diversity, cultured isolates allow us to link genomic potential to physiological processes, illuminate eco-evolutionary feedbacks, and test theories arising from comparative genomics of wild cells. Here, we report the isolation and characterization of novel low-light (LL) adapted Prochlorococcus strains that fill in multiple evolutionary gaps. These new strains are the first cultivated representatives of the LLVII and LLVIII paraphyletic grades of Prochlorococcus, which are broadly distributed in the lower regions of the ocean euphotic zone. Each of these grades is a unique, highly diverse section of the Prochlorococcus tree that separates distinct ecological groups: the LLVII grade branches between monophyletic clades that have facultatively particle-associated and constitutively planktonic lifestyles, while the LLVIII grade lies along the branch that leads to all high-light (HL) adapted clades. Characterizing strains and genomes from these grades yields insights into the large-scale evolution of Prochlorococcus. The new LLVII and LLVIII strains are adapted to growth at very low irradiance levels and possess unique light-harvesting gene signatures and pigmentation. The LLVII strains represent the most basal Prochlorococcus group with a major expansion in photosynthetic antenna genes. Further, a strain from the LLVIII grade challenges the paradigm that all LL-adapted Prochlorococcus exhibit high ratios of chl b:a2. These findings provide insights into major transitions in Prochlorococcus evolution, from the benthos to a fully planktonic lifestyle and from growth at low irradiances to the rise of the HL-adapted clades that dominate the modern ocean.

microbiology↗

Community-scale Synchronization and Temporal Partitioning of Gene Expression, Metabolism, and Lipid Biosynthesis in Oligotrophic Ocean Surface Waters

Sunlight drives daily rhythms of photosynthesis, growth, and division of photoautotrophs throughout the surface oceans. However, the cascading impacts of oscillatory light input on diverse microbial communities and community-scale metabolism remains unclear. Here we use an unsupervised machine learning approach to show that a small number of diel archetypes can explain pervasive periodic dynamics amongst more than 65,000 distinct time series, including transcriptional activity, macromolecules, lipids, and metabolites from the North Pacific Subtropical Gyre. Overall, we find evidence for synchronous timing of carbon-cycle gene expression that underlie daily oscillations in the concentrations of particulate organic carbon. In contrast, we find evidence of asynchronous timing in gene transcription related to nitrogen metabolism and related metabolic processes consistent with temporal niche partitioning amongst microorganisms in the bacterial and eukaryotic domains.

ecology↗

Combined pigment and metatranscriptomic analysis reveals synchronized diel patterns of phenotypic light response across domains in the open ocean

Sunlight is the most important environmental control on diel fluctuations in phytoplankton activity, and understanding diel microbial processes is essential to the study of oceanic biogeochemical cycles. Yet, little is known about the in situ frequency of phytoplankton metabolic activities and their coordination across different populations. We investigated the diel orchestration of phytoplankton activity involved in photosynthesis, photoacclimation, and photoprotection by analyzing the pigment and quinone distribution in combination with metatranscriptomes in the surface waters of the North Pacific Subtropical Gyre (NPSG). We found diel cycles in pigment abundances resulting from the balance of their synthesis and consumption. The night represents a metabolic recovery phase to refill cellular pigment stores, while the photosystems are remodeled towards photoprotection during the day. Transcript levels of genes involved in photosynthesis and pigment metabolism had highly synchronized diel expression patterns among all taxa, suggesting that there are similar regulatory mechanisms for light and energy metabolism across domains, and that other environmental factors drive niche differentiation. Observed decoupling of diel oscillations in transcripts and related pigments in the NPSG indicates that pigment abundance is modulated by environmental factors extending beyond gene expression/regulation, showing that metatranscriptomes may provide only limited insights on real-time photophysiological metabolism.

molecular biology↗

Metabolite composition of sinking particles reflects a changing microbial community and differential metabolite degradation

Marine sinking particles transport carbon from the surface and bury it in deep sea sediments where it can be sequestered on geologic time scales. The combination of the surface ocean food web that produces these particles and the particle-associated microbial community that degrades these particles, creates a complex set of variables that control organic matter cycling. We use targeted metabolomics to characterize a suite of small biomolecules, or metabolites, in sinking particles and compare their metabolite composition to that of the suspended particles in the euphotic zone from which they are likely derived. These samples were collected in the South Atlantic subtropical gyre, as well as in the equatorial Atlantic region and the Amazon River plume. The composition of targeted metabolites in the sinking particles was relatively similar throughout the transect, despite the distinct oceanic regions in which they were generated. Metabolites possibly derived from the degradation of nucleic acids and lipids, such as xanthine and glycine betaine, were an increased mole fraction of the targeted metabolites in the sinking particles relative to surface suspended particles, while algal-derived metabolites like the osmolyte dimethylsulfoniopropionate were a smaller fraction of the observed metabolites on the sinking particles. These compositional changes are shaped both by the removal of metabolites associated with detritus delivered from the surface ocean and by production of metabolites by the sinking particle-associated microbial communities. Further, they provide a basis for examining the types and quantities of metabolites that may be delivered to the deep sea by sinking particles.

microbiology↗