Edward F. DeLong

Oceanic microorganisms can rapidly respond to environmental variability. Determining how physical and biological processes control microbial distributions, abundances, and metabolic dynamics is challenging. Here, we used autonomous underwater vehicles capable of Lagrangian feature tracking and in situ sampling, in combination with ship-based measurements, to examine diel to weekly scale changes in microbial transcription and biogeochemistry in the deep chlorophyll maximum (DCM) of a mesoscale cyclonic eddy. Nearly 20% of total transcript expression showed diel periodicity, highlighting the importance of the diurnal cycle on phytoplankton metabolism in the dim waters of the DCM. Eddy-induced isopycnal uplift increased nutrient concentrations and caused upward displacement of the DCM, driving increased picoeukaryotic cell abundances and transcriptional activity of nitrate-incorporating photoautotrophs. As the eddy weakened, the DCM deepened and transcriptional activity shifted towards chemolithoautotrophic ammonia-oxidizing archaea. The temporal dynamics observed demonstrate how plankton communities rapidly respond to both diel variation and stochastic mesoscale disturbances.

Prokaryote seasonality is well documented in lakes, coastal areas, and inland seas, yet microbial annual periodicity in diverse open ocean settings is less well characterized. Here, we report seasonality in pelagic prokaryotes from open ocean depth profiles collected over 8.5 years in the North Pacific Subtropical Gyre. At depths shallower than 150 m, we found significant annual cycling in >62% of all pelagic prokaryote taxa. Although the proportion of seasonally cycling taxa diminished at depths >150 m, annual periodicity to depths of 4000 m was observed in some taxa. Even among closely related prokaryotes in the same clade, variable seasonal maxima were observed, a sub-clade-level temporal niche partitioning referred to here as seasonal ecotypes. One prevailing trend in the euphotic zone was a seasonal shift from surface water abundance maxima in winter, to spring and summer annual peaks at greater depths. In the upper mixed layer, most Prochlorococcus seasonal ecotypes had winter abundance maxima, while bacterial heterotrophs typically peaked in summer. In the euphotic subsurface, common seasonal ecotypes included Prochlorococcus having spring or summer maxima, and heterotrophic and chemolithoautotrophic prokaryotes having winter or fall maxima. At meso- and bathypelagic depths, most prokaryotes exhibited winter, spring, or fall seasonal maxima, alongside annual peaks of surface-dwelling photoautotrophs exported to the deep sea. The results indicate that seasonal ecotype annual cycling is a central feature of open ocean prokaryote communities, and suggest that subtle yet predictable seasonal niche partitioning helps drive and sustain prokaryote genetic diversification throughout the open ocean’s interior.

Mesoscale eddies, horizontally rotating currents sometimes referred to as “ocean weather,” influence open ocean macronutrient distributions, primary production, and microbial community structure. Such eddies impact ecosystems like the North Pacific Subtropical Gyre, where year-round thermal stratification limits the mixing of subsurface macronutrients with surface waters. Populations of the dominant primary producer Prochlorococcusin the North Pacific Subtropical Gyre consist of genetic variants with differential adaptive traits to light intensity, temperature, and macronutrient availability. How Prochlorococcuspopulation variants respond to transient, localized environmental changes, however, remains an open question. Leveraging microbial community phylogenetic, metagenomic, and metatranscriptomic data, we report here a consistent, specific enrichment of Prochlorococcushigh-light I ecotypes around the deep chlorophyll maximum in cyclonic eddies, but not adjacent anticyclonic eddies. The shallower deep chlorophyll maximum depths of cyclones had lower temperatures, higher light intensities, and elevated nutrient concentrations compared to adjacent anticyclones, which favored Prochlorococcushigh-light I ecotype proliferation. Prochlorococcushigh-light I ecotypes in the cyclone deep chlorophyll maximum exhibited unique genetic traits related to nitrogen metabolism and were enriched in gene transcripts associated with energy production, cell replication, and proliferation. Prochlorococcusgene transcripts involved in amino acid transport, metabolism, and biosynthesis were also elevated in the cyclone. These results suggest the potential importance of nitrogen metabolism in Prochlorococcushigh-light I ecotype proliferation in cyclonic eddies. Our findings demonstrate how mesoscale eddies shape microbial community structure in the oligotrophic ocean and how Prochlorococcuscommunities respond to short-term localized environmental variability.

Horizontal gene transfer (HGT) is enabled in part through the movement of DNA within two broad groups of small (7200 distinct chromosomal fragments and MGEs, many differentially partitioned between EVs and VLPs. Together these results suggest that distinctions in nanoparticle contents contribute to the mode and trajectory of microbial HGT networks and evolutionary dynamics in natural habitats.

Ocean eddies are mesoscale features that can extend > 100 km and maintain cohesiveness for months, impacting planktonic community structure and water column biogeochemical cycles. Standing stocks of protists in the water column and on sinking particles were investigated using microscopy, in situ imagery, and metabarcoding across an anticyclonic to cyclonic eddy dipole in the North Pacific Subtropical Gyre during July 2017. The water column was sampled from the surface to 500 m and particle interceptor traps were deployed at 150 m. Protistan assemblage composition varied substantially between sample type and analytical approach across the eddy dipole. Alveolates represented 63% of sequences from water samples. In contrast to water samples, rhizarian protists represented 79% of trap sequences obtained by metabarcoding of sediment trap material. Microscopy of trap material supported the important contribution of Rhizaria to sinking particles and revealed increased relative abundances of ciliates in the anticyclonic eddy and diatoms in the cyclonic eddy. In situ imagery confirmed the presence of relatively large Rhizaria that were not adequately assessed from water samples but contributed significantly to particle flux. Together, these data demonstrate differing perspectives of planktonic protistan community composition and contributions to sinking particles gained from the application of different sampling and analytic approaches. Our observations and analyses indicate a specific subset of the protistan community contributed disproportionately to organic matter downward export.

Horizontal gene transfer (HGT) is enabled in part through the movement of DNA within two broad groups of small (7200 diverse chromosomal fragments and MGEs, many differentially partitioned between EVs and VLPs. Together these results suggest that distinctions in nanoparticle contents contribute to the mode and trajectory of microbial HGT networks and evolutionary dynamics in natural habitats.

A considerable amount of particulate carbon produced by oceanic photosynthesis is exported to the deep-sea by the “gravitational pump” (~6.8 to 7.7 Pg C/year), sequestering it from the atmosphere for centuries. How particulate organic carbon (POC) is transformed during export to the deep sea however is not well understood. Here, we report that dominant suspended prokaryotes also found in sinking particles serve as informative tracers of particle export processes. In a three-year time series from oceanographic campaigns in the Pacific Ocean, upper water column relative abundances of suspended prokaryotes entrained in sinking particles decreased exponentially from depths of 75 to 250 m, conforming to known depth-attenuation patterns of carbon, energy, and mass fluxes in the epipelagic zone. Below ~250 m however, the relative abundance of suspended prokaryotes entrained in sinking particles increased with depth. These results indicate that microbial entrainment, colonization, and sinking particle formation are elevated at mesopelagic and bathypelagic depths. Comparison of suspended and sinking particle-associated microbes provides information about the depth-variability of POC export and biotic processes, that is not evident from biogeochemical data alone.

Phage satellites are mobile genetic elements that propagate by parasitizing bacteriophage replication. We report here the discovery of abundant and diverse phage satellites that were packaged as concatemeric repeats within naturally occurring bacteriophage particles in seawater. These same phage-parasitizing mobile elements were found integrated in the genomes of dominant co-occurring bacterioplankton species. Like known phage satellites, many marine phage satellites encoded genes for integration, DNA replication, phage interference, and capsid assembly. Many also contained distinctive gene suites indicative of unique virus hijacking, phage immunity, and mobilization mechanisms. Marine phage satellite sequences were widespread in local and global oceanic virioplankton populations, reflecting their ubiquity, abundance, and temporal persistence in marine planktonic communities worldwide. Their gene content and putative life cycles suggest they may impact host-cell phage immunity and defense, lateral gene transfer, bacteriophage-induced cell mortality and cellular host and virus productivity. Given that marine phage satellites cannot be distinguished from bona fide viral particles via commonly used microscopic techniques, their predicted numbers (∼3.2 × 10 ²⁶ in the ocean) may influence current estimates of virus densities, production, and virus-induced mortality. In total, the data suggest that marine phage satellites have potential to significantly impact the ecology and evolution of bacteria and their viruses throughout the oceans. We predict that any habitat that harbors bacteriophage will also harbor similar phage satellites, making them a ubiquitous feature of most microbiomes on Earth.

Particle-attached microbes play large roles in the ocean carbon cycle and help to sequester atmospheric CO ₂ and to deliver nutrients and energy on sinking particles to the deep sea. Here, we report on the genomic traits of particle-attached versus free-living microbes throughout the ocean water column to better differentiate their specific metabolic and ecological roles in the sea.