Transport-limited reactions in microbial systems.

Predicting microbial metabolic rates and emergent biogeochemical fluxes remains challenging due to the many unknown population dynamical, physiological and reaction-kinetic parameters and uncertainties in species composition. Here, we show that the need for these parameters can be eliminated when population dynamics and reaction kinetics operate at much shorter time scales than physical mixing processes. Such scenarios are widespread in poorly mixed water columns and sediments. In this 'fast-reaction-transport' (FRT) limit, all that is required for predictions are chemical boundary conditions, the physical mixing processes and reaction stoichiometries, while no knowledge of species composition, physiology or population/reaction kinetic parameters is needed. Using time-series data spanning years 2001-2014 and depths 180-900 m across the permanently anoxic Cariaco Basin, we demonstrate that the FRT approach can accurately predict the dynamics of major electron donors and acceptors (Pearson r ≥ 0.9 in all cases). Hence, many microbial processes in this system are largely transport limited and thus predictable regardless of species composition, population dynamics and kinetics. Our approach enables predictions for many systems in which microbial community dynamics and kinetics are unknown. Our findings also reveal a mechanism for the frequently observed decoupling between function and taxonomy in microbial systems.

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.

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.

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.

Free-living chemoautotrophic and particle-attached heterotrophic prokaryotes dominate microbial assemblages along a pelagic redox gradient.

Using the anoxic Cariaco Basin as a natural laboratory, particle association of bacterial and archaeal taxa was assessed by iTag sequencing and qPCR gene assays of samples spanning an oxic-anoxic-euxinic gradient. A total of 10%-12% of all bacterial and archaeal cells were found in the particle-associated (PA) fraction, operationally defined as prokaryotes captured on 2.7 µm membranes. Both redox condition and size fraction segregated bacterial taxa. Archaeal taxa varied according to redox conditions, but were similar between size fractions. Taxa putatively associated with chemoautotrophic sulfur oxidation and nitrification dominated the free-living (FL) fraction throughout the oxycline (< 1-120 µM O2 ) and upper anoxic layer. Bacteria in the oxycline's PA fraction included taxa known to be aerobic and anaerobic chemoorganotrophs. At shallow anoxic depths, PA taxa were primarily affiliated with anaerobic sulfate ( SO42-)-reducing lineages. PA fractions in the most sulfidic samples were dominated by taxa affiliated with CH4 oxidizing, fermenting and SO42- reducing lineages. Prevalence of particle-associated SO42--reducing taxa and abundant sulfur-oxidizing taxa in both size fractions across the oxic-anoxic interface is consistent with the cryptic sulfur cycling concept. Bacterial assemblage diversity in the PA fraction always exceeded the FL fraction except in the most oxic samples, whereas Archaeal diversity was not consistently different between size fractions. Our results suggest that these particle-associated and free-living bacterial assemblages are functionally different and that the interplay between particle microhabitats and surrounding geochemical regimes is a strong selective force shaping microbial communities throughout the water column.

Spatial variability of Spanish sardine (Sardinella aurita) abundance as related to the upwelling cycle off the southeastern Caribbean Sea.

The Sardinella aurita fishery off northeastern Venezuela, region of seasonal wind-driven coastal-upwelling, accounts for 90% of the Caribbean Sea small pelagic catch. This law-protected artisanal fishery takes place up to ~10 km offshore. The spatial distribution, number of schools, and biomass of S. aurita were studied using eight hydro-acoustic surveys (1995-1998). The study included the analysis of satellite-derived sea surface temperature and chlorophyll-a. Surveys were grouped by strong, weak, and transitional upwelling seasons. Relationships between these observations were analyzed using Generalized Additive Models. Results show that during the primary upwelling season (January-May) sardines were widely distributed in upwelling plumes that extended up to 70 km offshore. In the other hand, during the weak upwelling season (September-October) higher sardine densities were found within 10 Km off the coastal upwelling foci. The number of small pelagic schools was directly correlated with small pelagic densities; however, regardless of the season, higher numbers of small pelagic schools were always closer to the shoreline, especially during warm conditions. These two behaviors increase the availability and catchability of sardines for the artisanal fishery during the warm season, regardless of the total stock size. Using this evidence, we pose the hypothesis that the collapse of the regional S. aurita fishery in 2005 was due to a combination of stressful habitat conditions sustained since 2004. These included bottom-up factors due to food scarcity caused by weak upwelling, combined with top-down stress due to overfishing, as sardines accumulated in narrow diminished upwelling plumes located close to the coast. The increased catchability within easily accessible upwelling foci led to the demise of this biological resource, which as of 2014 had not yet recovered. Environmental conditions affecting the sardine habitat needs to be taken into account for the management of this stock. For example, during years with weak upwelling, special measures should be taken during the warm season on the second half of the year to avoid further pressure on the stock.

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.

Denaturing gradient gel electrophoresis analyses of the vertical distribution and diversity of Vibrio spp. populations in the Cariaco Basin.

The Cariaco system is the second largest permanently anoxic marine water body in the world. Its water column is characterized by a pronounced vertical layering of microbial communities. The goal of our study was to investigate the vertical distribution and diversity of Vibrio spp. present in the Cariaco Basin waters using denaturing gradient gel electrophoresis (DGGE) of PCR-amplified 16S rDNA fragments. Representatives of the Vibrio genus were detected by nested and direct PCR in seawater at 10 depths. Sequence analyses of 55 DGGE bands revealed that only 11 different operational taxonomic units (OTU) are identified as Vibrio species. Between one and five OTUs were detected at each depth and the most common OTUs were OTU 1 and OTU 2, which phylogenetically clustered with Vibrio chagasii and Vibrio fortis, respectively. OTUs 3 and 4 were only found in the anoxic zone and were identified as Vibrio orientalis and Vibrio neptunius, respectively. Several Vibrio species detected are potentially pathogenic to human, prawns and corals such as Vibrio parahaemolyticus, Vibrio fischeri and Vibrio shilonii. In the Cariaco Basin, different Vibrio species were found to be specific to specific depths strata, suggesting that this genus is a natural component of the microbial communities in this marine redox environment.

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.