Circumventing kinetics in biogeochemical modeling.

Microbial metabolism drives biogeochemical fluxes in virtually every ecosystem. Modeling these fluxes is challenged by the incredible diversity of microorganisms, whose kinetic parameters are largely unknown. In poorly mixed systems, such as stagnant water columns or sediments, however, long-term bulk microbial metabolism may become limited by physical transport rates of substrates across space. Here we mathematically show that under these conditions, biogeochemical fluxes are largely predictable based on the system's transport properties, chemical boundary conditions, and the stoichiometry of metabolic pathways, regardless of the precise kinetics of the resident microorganisms. We formalize these considerations into a predictive modeling framework and demonstrate its use for the Cariaco Basin subeuphotic zone, one of the largest anoxic marine basins worldwide. Using chemical concentration data solely from the upper boundary (depth 180 m) and lower boundary (depth 900 m), but without a priori knowledge of metabolite fluxes, chemical depth profiles, kinetic parameters, or microbial species composition, we predict the concentrations and vertical fluxes of biologically important substances, including oxygen, nitrate, hydrogen sulfide, and ammonium, across the entire considered depth range (180-900 m). Our predictions largely agree with concentration measurements over a period of 14 years ([Formula: see text] = 0.78-0.92) and become particularly accurate during a period where the system was near biogeochemical steady state (years 2007-2009, [Formula: see text] = 0.86-0.95). Our work enables geobiological predictions for a large class of ecosystems without knowledge of kinetic parameters or geochemical depth profiles. Conceptually, our work provides a possible explanation for the decoupling between microbial species composition and bulk metabolic function, observed in various ecosystems.

Diverse nitrogen cycling pathways across a marine oxygen gradient indicate nitrogen loss coupled to chemoautotrophic activity.

Genetic markers and geochemical assays of microbial nitrogen cycling processes, including autotrophic and heterotrophic denitrification, anammox, ammonia oxidation, and nitrite oxidation, were examined across the oxycline, suboxic, and anoxic zones of the Cariaco Basin, Venezuela. Ammonia and nitrite oxidation genes were expressed through the entire gradient. Transcripts associated with autotrophic and heterotrophic denitrifiers were mostly confined to the suboxic zone and below but were also present in particles in the oxycline. Anammox genes and transcripts were detected over a narrow depth range near the bottom of the suboxic zone and coincided with secondary NO2 - maxima and available NH4 + . Dissolved inorganic nitrogen (DIN) amendment incubations and comparisons between our sampling campaigns suggested that denitrifier activity may be closely coupled with NO3 - availability. Expression of denitrification genes at depths of high rates of chemoautotrophic carbon fixation and phylogenetic analyses of nitrogen cycling genes and transcripts indicated a diverse array of denitrifiers, including chemoautotrophs capable of using NO3 - to oxidize reduced sulfur species. Thus, results suggest that the Cariaco Basin nitrogen cycle is influenced by autotrophic carbon cycling in addition to organic matter oxidation and anammox.

Ecosystem responses in the southern Caribbean Sea to global climate change.

Over the last few decades, rising greenhouse gas emissions have promoted poleward expansion of the large-scale atmospheric Hadley circulation that dominates the Tropics, thereby affecting behavior of the Intertropical Convergence Zone (ITCZ) and North Atlantic Oscillation (NAO). Expression of these changes in tropical marine ecosystems is poorly understood because of sparse observational datasets. We link contemporary ecological changes in the southern Caribbean Sea to global climate change indices. Monthly observations from the CARIACO Ocean Time-Series between 1996 and 2010 document significant decadal scale trends, including a net sea surface temperature (SST) rise of ∼1.0 ± 0.14 °C (±SE), intensified stratification, reduced delivery of upwelled nutrients to surface waters, and diminished phytoplankton bloom intensities evident as overall declines in chlorophyll a concentrations (ΔChla = -2.8 ± 0.5%⋅y(-1)) and net primary production (ΔNPP = -1.5 ± 0.3%⋅y(-1)). Additionally, phytoplankton taxon dominance shifted from diatoms, dinoflagellates, and coccolithophorids to smaller taxa after 2004, whereas mesozooplankton biomass increased and commercial landings of planktivorous sardines collapsed. Collectively, our results reveal an ecological state change in this planktonic system. The weakening trend in Trade Winds (-1.9 ± 0.3%⋅y(-1)) and dependent local variables are largely explained by trends in two climatic indices, namely the northward migration of the Azores High pressure center (descending branch of Hadley cell) by 1.12 ± 0.42°N latitude and the northeasterly progression of the ITCZ Atlantic centroid (ascending branch of Hadley cell), the March position of which shifted by about 800 km between 1996 and 2009.

Microbial metabolite fluxes in a model marine anoxic ecosystem.

Permanently anoxic regions in the ocean are widespread and exhibit unique microbial metabolic activity exerting substantial influence on global elemental cycles and climate. Reconstructing microbial metabolic activity rates in these regions has been challenging, due to the technical difficulty of direct rate measurements. In Cariaco Basin, which is the largest permanently anoxic marine basin and an important model system for geobiology, long-term monitoring has yielded time series for the concentrations of biologically important compounds; however, the underlying metabolite fluxes remain poorly quantified. Here, we present a computational approach for reconstructing vertical fluxes and in situ net production/consumption rates from chemical concentration data, based on a 1-dimensional time-dependent diffusive transport model that includes adaptive penalization of overfitting. We use this approach to estimate spatiotemporally resolved fluxes of oxygen, nitrate, hydrogen sulfide, ammonium, methane, and phosphate within the sub-euphotic Cariaco Basin water column (depths 150-900 m, years 2001-2014) and to identify hotspots of microbial chemolithotrophic activity. Predictions of the fitted models are in excellent agreement with the data and substantially expand our knowledge of the geobiology in Cariaco Basin. In particular, we find that the diffusivity, and consequently fluxes of major reductants such as hydrogen sulfide, and methane, is about two orders of magnitude greater than previously estimated, thus resolving a long-standing apparent conundrum between electron donor fluxes and measured dark carbon assimilation rates.

The Scientific Legacy of the CARIACO Ocean Time-Series Program.

The CARIACO (Carbon Retention in a Colored Ocean) Ocean Time-Series Program station, located at 10.50°N, 64.66°W, observed biogeochemical and ecological processes in the Cariaco Basin of the southwestern Caribbean Sea from November 1995 to January 2017. The program completed 232 monthly core cruises, 40 sediment trap deployment cruises, and 40 microbiogeochemical process cruises. Upwelling along the southern Caribbean Sea occurs from approximately November to August. High biological productivity (320-628 g C m-2 y-1) leads to large vertical fluxes of particulate organic matter, but only approximately 9-10 g C m-2 y-1 fall to the bottom sediments (∼1-3% of primary production). A diverse community of heterotrophic and chemoautotrophic microorganisms, viruses, and protozoa thrives within the oxic-anoxic interface. A decrease in upwelling intensity from approximately 2003 to 2013 and the simultaneous overfishing of sardines in the region led to diminished phytoplankton bloom intensities, increased phytoplankton diversity, and increased zooplankton densities. The deepest waters of the Cariaco Basin exhibited long-term positive trends in temperature, salinity, hydrogen sulfide, ammonia, phosphate, methane, and silica. Earthquakes and coastal flooding also resulted in the delivery of sediment to the seafloor. The program's legacy includes climate-quality data from suboxic and anoxic habitats and lasting relationships between international researchers.

The Diversity of Sulfide Oxidation and Sulfate Reduction Genes Expressed by the Bacterial Communities of the Cariaco Basin, Venezuela.

Qualitative expression of dissimilative sulfite reductase (dsrA), a key gene in sulfate reduction, and sulfide:quinone oxidoreductase (sqr), a key gene in sulfide oxidation was investigated. Neither of the two could be amplified from mRNA retrieved with Niskin bottles but were amplified from mRNA retrieved by the Deep SID. The sqr and sqr-like genes retrieved from the Cariaco Basin were related to the sqr genes from a Bradyrhizobium sp., Methylomicrobium alcaliphilum, Sulfurovum sp. NBC37-1, Sulfurimonas autotrophica, Thiorhodospira sibirica and Chlorobium tepidum. The dsrA gene sequences obtained from the redoxcline of the Cariaco Basin belonged to chemoorganotrophic and chemoautotrophic sulfate and sulfur reducers belonging to the class Deltaproteobacteria (phylum Proteobacteria) and the order Clostridiales (phylum Firmicutes).

The dynamics of the bacterial diversity in the redox transition and anoxic zones of the Cariaco Basin assessed by parallel tag sequencing.

Massively parallel tag sequencing was applied to describe the bacterial diversity in the redox transition and anoxic zones of the Cariaco Basin. In total, 14 samples from the Cariaco Basin were collected over a period of eight years from two stations. A total of 244 357 unique bacterial V6 amplicons were sequenced. The total number of operational taxonomic units (OTUs) found in this study was 4692, with a range of 511-1491 OTUs per sample. Approximately 95% of the OTUs found in the redox transition zone and anoxic layers of Cariaco are represented by less than 50 amplicons suggesting that only about 5% of the bacterial OTUs are responsible for the bulk of the microbial processes in the basin redox transition and anoxic zones. The same dominant OTUs were observed across all eight years of sampling although periodic fluctuations in their proportion were apparent. No distinctive differences were observed between the bacterial communities from the redox transition and anoxic layers of the Cariaco Basin water column. The largest proportion of amplicons belongs to Gammaproteobacteria represented mostly by sulfide oxidizers, followed by Marine Group A (originally described as SAR406; Gordon and Giovannoni 1996), a group of uncultured bacteria hypothesized to be involved in metal reduction, and sulfate-reducing Deltaproteobacteria. Gammaproteobacteria, Deltaproteobacteria and Marine Group A make up 67-90% of all V6 amplicons sequenced in this study. This strongly suggests that the basin's microbial communities are actively involved in the sulfur-related metabolism and coupling of the sulfur and carbon cycles. According to detrended canonical correspondence analysis, ecological factors such as chemoautotrophy, nitrate and oxidized and reduced sulfur compounds influence the structuring and distribution of the Cariaco microbial communities.

Bacterial community composition in a large marine anoxic basin: a Cariaco Basin time-series survey.

Redox transition zones play a crucial role in biogeochemical cycles of several major elements. Because microorganisms mediate many reactions of these cycles, they actively participate in establishing geochemical gradients. In turn, the geochemical gradients structure microbial communities. We studied the interrelationship between the bacterial community structure and the geochemical gradient in the Cariaco Basin, the largest truly marine anoxic basin. This study's dataset includes bacterial community composition in 113 water column samples as well as the data for environmental variables (gradients of oxygen, hydrogen sulfide, sulfite, thiosulfate, ammonia, nitrate, nitrite, dissolved manganese and iron, dark CO2 fixation, and bacterial abundance) collected between 1997 and 2006. Several prominent bacterial groups are present throughout the entire water column. These include members of Gamma-, Delta-, and Epsilonproteobacteria, as well as members of the Marine Group A, the candidate divisions OP11 and Car731c. Canonical correspondence analysis indicated that microbial communities segregate along vectors representing oxygenated conditions, nitrite, nitrate and anoxic environments represented by chemoautotrophy, ammonia, sulfite, and hydrogen sulfide.

Comparison of vertical distributions of prokaryotic assemblages in the anoxic Cariaco Basin and Black Sea by use of fluorescence in situ hybridization.

Individual prokaryotic cells from two major anoxic basins, the Cariaco Basin and the Black Sea, were enumerated throughout their water columns using fluorescence in situ hybridization (FISH) with the fluorochrome Cy3 or horseradish peroxidase-modified oligonucleotide probes. For both basins, significant differences in total prokaryotic abundance and phylogenetic composition were observed among oxic, anoxic, and transitional (redoxcline) waters. Epsilon-proteobacteria, Crenarchaeota, and Euryarchaeota were more prevalent in the redoxclines, where previous studies reported high rates of chemoautotrophic production relative to those in waters above and below the redoxclines. Relative abundances of Archaea in both systems varied between 1% and 28% of total prokaryotes, depending on depth. The prokaryotic community composition varied between the two anoxic basins, consistent with distinct geochemical and physical conditions. In the Black Sea, the relative contributions of group I Crenarchaeota (median, 5.5%) to prokaryotic communities were significantly higher (P < 0.001; n = 20) than those of group II Euryarchaeota (median, 2.9%). In contrast, their proportions were nearly equivalent in the Cariaco Basin. Beta-proteobacteria were unexpectedly common throughout the Cariaco Basin's water column, accounting for an average of 47% of 4',6'-diamidino-2-phenylindole (DAPI)-stained cells. This group was below the detection limit (<1%) in the Black Sea samples. Compositional differences between basins may reflect temporal variability in microbial populations and/or systematic differences in environmental conditions and the populations for which they select.