Victoria J. Coles

Changes in Antarctic Bottom Water properties in the western South Atlantic in the late 1980s

Data collected in 1988–1989, as part of the South Atlantic Ventilation Experiment, have been combined with the historical database to study the circulation and water mass variability of the abyssal water in the Argentine Basin. A map of potential temperature at 4000 m used as an indication of geostrophic shear defines a south and western intensified crescent-shaped abyssal recirculation. Within this recirculation, and its northward extension to the Brazil Basin, Antarctic Bottom Water (AABW) properties have undergone two modifications during the 1980s: (1) The water mass cooled (0.05°C) and freshened (0.008 in salinity ratio) on surfaces of constant density. (2) The densest layer of AABW was altered to less dense water through mixing or advection out of the study area. This water mass change does not appear to have affected the flow pattern. Data collected in 1983 and 1988 to the north in the Brazil Basin show penetration of the freshwater mass in the deep western boundary current to between 18°S and 10°S, indicating very rapid propagation of the anomaly from the Argentine Basin into the Brazil Basin as a deep western boundary current. It is suggested that open ocean convective events within the Weddell Sea contributed to the change in AABW documented here.

Microspatial gene expression patterns in the Amazon River Plume

Significance The microbial community of the Amazon River Plume determines the fate of the world’s largest input of terrestrial carbon and nutrients to the ocean. By benchmarking with internal standards during sample collection, we determined that each liter of plume seawater contains 1 trillion genes and 50 billion transcripts from thousands of bacterial, archaeal, and eukaryotic taxa. Gene regulation by taxa inhabiting distinct microenvironments provides insights into micron-scale patterns of transformations in the marine carbon, nitrogen, phosphorus, and sulfur cycles in this globally important ecosystem. We investigated expression of genes mediating elemental cycling at the microspatial scale in the ocean’s largest river plume using, to our knowledge, the first fully quantitative inventory of genes and transcripts. The bacterial and archaeal communities associated with a phytoplankton bloom in Amazon River Plume waters at the outer continental shelf in June 2010 harbored ∼1.0 × 1013 genes and 4.7 × 1011 transcripts per liter that mapped to several thousand microbial genomes. Genomes from free-living cells were more abundant than those from particle-associated cells, and they generated more transcripts per liter for carbon fixation, heterotrophy, nitrogen and phosphorus uptake, and iron acquisition, although they had lower expression ratios (transcripts⋅gene−1) overall. Genomes from particle-associated cells contributed more transcripts for sulfur cycling, aromatic compound degradation, and the synthesis of biologically essential vitamins, with an overall twofold up-regulation of expression compared with free-living cells. Quantitatively, gene regulation differences were more important than genome abundance differences in explaining why microenvironment transcriptomes differed. Taxa contributing genomes to both free-living and particle-associated communities had up to 65% of their expressed genes regulated differently between the two, quantifying the extent of transcriptional plasticity in marine microbes in situ. In response to patchiness in carbon, nutrients, and light at the micrometer scale, Amazon Plume microbes regulated the expression of genes relevant to biogeochemical processes at the ecosystem scale.

Patterns of Transcript Abundance of Eukaryotic Biogeochemically-Relevant Genes in the Amazon River Plume.

The Amazon River has the largest discharge of all rivers on Earth, and its complex plume system fuels a wide array of biogeochemical processes, across a large area of the western tropical North Atlantic. The plume thus stimulates microbial processes affecting carbon sequestration and nutrient cycles at a global scale. Chromosomal gene expression patterns of the 2.0 to 156 μm size-fraction eukaryotic microbial community were investigated in the Amazon River Plume, generating a robust dataset (more than 100 million mRNA sequences) that depicts the metabolic capabilities and interactions among the eukaryotic microbes. Combining classical oceanographic field measurements with metatranscriptomics yielded characterization of the hydrographic conditions simultaneous with a quantification of transcriptional activity and identity of the community. We highlight the patterns of eukaryotic gene expression for 31 biogeochemically significant gene targets hypothesized to be valuable within forecasting models. An advantage to this targeted approach is that the database of reference sequences used to identify the target genes was selectively constructed and highly curated optimizing taxonomic coverage, throughput, and the accuracy of annotations. A coastal diatom bloom highly expressed nitrate transporters and carbonic anhydrase presumably to support high growth rates and enhance uptake of low levels of dissolved nitrate and CO2. Diatom-diazotroph association (DDA: diatoms with nitrogen fixing symbionts) blooms were common when surface salinity was mesohaline and dissolved nitrate concentrations were below detection, and hence did not show evidence of nitrate utilization, suggesting they relied on ammonium transporters to aquire recently fixed nitrogen. These DDA blooms in the outer plume had rapid turnover of the photosystem D1 protein presumably caused by photodegradation under increased light penetration in clearer waters, and increased expression of silicon transporters as silicon became limiting. Expression of these genes, including carbonic anhydrase and transporters for nitrate and phosphate, were found to reflect the physiological status and biogeochemistry of river plume environments. These relatively stable patterns of eukaryotic transcript abundance occurred over modest spatiotemporal scales, with similarity observed in sample duplicates collected up to 2.45 km in space and 120 minutes in time. These results confirm the use of metatranscriptomics as a valuable tool to understand and predict microbial community function.

Indonesian throughflow nutrient fluxes and their potential impact on Indian Ocean productivity

The Indonesian throughflow (ITF) is a chokepoint in the upper ocean thermohaline circulation, carrying Pacific waters through the strongly mixed Indonesian Seas and into the Indian Ocean. Yet the influence of the ITF on biogeochemical fluxes into the Indian Ocean is largely unknown. This study determines the first depth- and time-resolved nitrate, phosphate, and silicate fluxes at the three main exit passages of the ITF: Lombok Strait, Ombai Strait, and Timor Passage. Nutrient flux as well as its variability with depth and time differs greatly between the passages. We estimate the effective flux of nutrients into the Indian Ocean by accounting for existing nutrients in the basin and find it largest in the upper 300–400 m. This suggests that the majority of ITF nutrient supply to the Indian Ocean is to thermocline waters, where it is likely to support new production and significantly impact Indian Ocean biogeochemical cycling.

Research Opportunities and Challenges in the Indian Ocean

The Indian Ocean is a dynamically complex and highly variable system, with circulation features and biogeochemical properties that are unusual in many respects. Yet the Indian Ocean (IO) remains one of the most undersampled and least understood of the worlds ocean basins. In this article, we define several outstanding research questions that need to be addressed in the IO related to ocean currents and variability, the controls and fate of primary production, global change and anthropogenic impacts, and the role of higher trophic levels in ecological processes and biogeochemical cycles. We also discuss a unique opportunity that has recently arisen for staging research in the IO.

Bacterial Biogeography across the Amazon River-Ocean Continuum

Spatial and temporal patterns in microbial biodiversity across the Amazon river-ocean continuum were investigated along ∼675 km of the lower Amazon River mainstem, in the Tapajós River tributary, and in the plume and coastal ocean during low and high river discharge using amplicon sequencing of 16S rRNA genes in whole water and size-fractionated samples (0.2–2.0 μm and >2.0 μm). River communities varied among tributaries, but mainstem communities were spatially homogeneous and tracked seasonal changes in river discharge and co-varying factors. Co-occurrence network analysis identified strongly interconnected river assemblages during high (May) and low (December) discharge periods, and weakly interconnected transitional assemblages in September, suggesting that this system supports two seasonal microbial communities linked to river discharge. In contrast, plume communities showed little seasonal differences and instead varied spatially tracking salinity. However, salinity explained only a small fraction of community variability, and plume communities in blooms of diatom-diazotroph assemblages were strikingly different than those in other high salinity plume samples. This suggests that while salinity physically structures plumes through buoyancy and mixing, the composition of plume-specific communities is controlled by other factors including nutrients, phytoplankton community composition, and dissolved organic matter chemistry. Co-occurrence networks identified interconnected assemblages associated with the highly productive low salinity near-shore region, diatom-diazotroph blooms, and the plume edge region, and weakly interconnected assemblages in high salinity regions. This suggests that the plume supports a transitional community influenced by immigration of ocean bacteria from the plume edge, and by species sorting as these communities adapt to local environmental conditions. Few studies have explored patterns of microbial diversity in tropical rivers and coastal oceans. Comparison of Amazon continuum microbial communities to those from temperate and arctic systems suggest that river discharge and salinity are master variables structuring a range of environmental conditions that control bacterial communities across the river-ocean continuum.

Ocean biogeochemistry modeled with emergent trait-based genomics

Functional ocean biogeography Marine ecosystems are well represented in metagenomic and transcriptomic data. These data are not routinely used to test ecosystem models that explore ocean biogeography or biogeochemistry. Coles et al. built a model in which genes for a range of functions were assigned to different suites of simulated microbes (see the Perspective by Rynearson). Communities emerged from the model with realistic biogeographical and biogeochemical profiles when compared to microbial data collected from the Amazon River plume. However, functional composition trumped the details of taxonomy, and different, coevolving community compositions emerged that provided similar biogeochemical outcomes. Science, this issue p. 1149; see also p. 1129 Results of genomic-based microbe community modeling resemble real-world observations from the Amazon River plume. Marine ecosystem models have advanced to incorporate metabolic pathways discovered with genomic sequencing, but direct comparisons between models and “omics” data are lacking. We developed a model that directly simulates metagenomes and metatranscriptomes for comparison with observations. Model microbes were randomly assigned genes for specialized functions, and communities of 68 species were simulated in the Atlantic Ocean. Unfit organisms were replaced, and the model self-organized to develop community genomes and transcriptomes. Emergent communities from simulations that were initialized with different cohorts of randomly generated microbes all produced realistic vertical and horizontal ocean nutrient, genome, and transcriptome gradients. Thus, the library of gene functions available to the community, rather than the distribution of functions among specific organisms, drove community assembly and biogeochemical gradients in the model ocean.

Inertial gyre solutions from a primitive equation ocean model

A numerical exploration of inertial equilibrium states obtained with a primitive equation ocean model suggests that they can be described using statistical mechanics theory developed in the framework of quasi-geostrophy. The performance of the numerical model is first assessed with respect to the quasi-geostrophic model considering a series of experiments in the quasi-geostrophic range, in a closed basin with flat bottom and varying Rossby numbers. The results show that our model is consistent with the quasi-geostrophic model even in terms of dependence from boundary conditions and eddy viscosity values, and that the free surface contribution is negligible. As in the quasi-geostrophic experiments, a tendency toward Fofonoff flows is observed. This tendency remains in a second series of experiments performed outside the quasi-geostrophic range, namely with flows with higher Rossby numbers and with steep topography, characterized by sloping boundaries with an order one fractional change in the depth. It is only close to the boundaries that ageostrophic effects modify the flows. In conclusion, the fact that statistical mechanics theory, initially developed in the framework of quasi-geostrophy, holds for more realistic flows with steep topography supports development of subgrid scale parameterizations based on statistical mechanics theory, to be used in realistic general circulation models.

Expression patterns of elemental cycling genes in the Amazon River Plume

Metatranscriptomics and metagenomics data sets benchmarked with internal standards were used to characterize the expression patterns for biogeochemically relevant bacterial and archaeal genes mediating carbon, nitrogen, phosphorus and sulfur uptake and metabolism through the salinity gradient of the Amazon River Plume. The genes were identified in 48 metatranscriptomic and metagenomic data sets summing to >500 million quality-controlled reads from six locations in the plume ecosystem. The ratio of transcripts per gene copy (a direct measure of expression made possible by internal standard additions) showed that the free-living bacteria and archaea exhibited only small changes in the expression levels of biogeochemically relevant genes through the salinity and nutrient zones of the plume. In contrast, the expression levels of genes in particle-associated cells varied over orders of magnitude among the stations, with the largest differences measured for genes mediating aspects of nitrogen cycling (nifH, amtB and amoA) and phosphorus acquisition (pstC, phoX and phoU). Taxa varied in their baseline gene expression levels and extent of regulation, and most of the spatial variation in the expression level could be attributed to changes in gene regulation after removing the effect of shifting taxonomic composition. We hypothesize that changes in microbial element cycling along the Amazon River Plume are largely driven by shifting activities of particle-associated cells, with most activities peaking in the mesohaline regions where N2 fixation rates are elevated.

Approaches and Challenges for Linking Marine Biogeochemical Models with the “Omics” Revolution

An unnecessary divide separates the marine biogeochemical modeling and omics research communities that impedes the utilization of new omics data in the development and validation of large-scale, three-dimensional, coupled physical–biogeochemical models. To close this gap we have to: (1) bridge the scientific, cultural, and structural divide that separates the marine biogeochemical modeling and omics research communities preventing scientific exchange and collaboration; (2) develop techniques for relating omics data to aspects of our current biogeochemical model structures and functions that allow useful comparisons between the models and the data; and (3) mobilize development of models that are more representative of the diverse microbial community composition and the associated diversity of metabolic functions that exists in marine waters so that this mapping can be realized to a greater degree. An important caveat here is that the latter may lead to the development of increasingly complex models, which creates both computational and validation challenges.