The microbiome of the Black Sea water column analyzed by shotgun and genome centric metagenomics

Background The Black Sea is the largest brackish water body in the world, although it is connected to the Mediterranean Sea and presents an upper water layer similar to some regions of the former, albeit with lower salinity and temperature. Despite its well-known hydrology and physicochemical features, this enormous water mass remains poorly studied at the microbial genomics level. Results We have sampled its different water masses and analyzed the microbiome by shotgun and genome-resolved metagenomics, generating a large number of metagenome-assembled genomes (MAGs) from them. We found various similarities with previously described Black Sea metagenomic datasets, that show remarkable stability in its microbiome. Our datasets are also comparable to other marine anoxic water columns like the Cariaco Basin. The oxic zone resembles to standard marine (e.g. Mediterranean) photic zones, with Cyanobacteria (Synechococcus but a conspicuously absent Prochlorococcus), and photoheterotrophs domination (largely again with marine relatives). The chemocline presents very different characteristics from the oxic surface with many examples of chemolithotrophic metabolism (Thioglobus) and facultatively anaerobic microbes. The euxinic anaerobic zone presents, as expected, features in common with the bottom of meromictic lakes with a massive dominance of sulfate reduction as energy-generating metabolism, a few (but detectable) methanogenesis marker genes, and a large number of “dark matter” streamlined genomes of largely unpredictable ecology. Conclusions The Black Sea oxic zone presents many similarities to the global ocean while the redoxcline and euxinic water masses have similarities to other similar aquatic environments of marine (Cariaco Basin or other Black Sea regions) or freshwater (meromictic monimolimnion strata) origin. The MAG collection represents very well the different types of metabolisms expected in this kind of environment. We are adding critical information about this unique and important ecosystem and its microbiome.

Millennial-Scale Environmental Variability in Late Quaternary Deep-Sea Sediments from the Demerara Rise, NE Coast of South America

We carried out a rock magnetic study of two deep-sea gravity cores from the Demerara Rise, NE South America. Our previous studies provided radiocarbon and paleomagnetic chronologies for these cores. This study presents detailed rock magnetic measurements on these cores in order to characterize the rock magnetic mineralogy and grain size as indicators of the overall clastic fraction. We measured the magnetic susceptibility, anhysteretic remanence, and isothermal remanence and demagnetized the remanences at several alternating field demagnetization levels. The magnetic intensities estimate the magnetic material concentration (and indirectly the overall clastic fraction) in the cores. Ratios of rock magnetic parameters indicate the relative grain size of the magnetic material (and indirectly the overall clastic grain size). Rock magnetic intensity parameters and rock magnetic ratios both vary systematically and synchronously over the last 30,000 years in both cores. There is a multi-millennial-scale cyclicity, with intervals of high magnetic intensity (high magnetic and clastic content) with low magnetic ratios (coarser magnetic and clastic grain size), alternating in sequence with intervals of low magnetic intensity with high magnetic ratios (finer grain size). There is also a higher-frequency millennial-scale variability in intensity superposed on the multi-millennial-scale variability. There are nine (A–I) multi-millennial-scale intervals in the cores. Intervals A, C, E, G, and I have high magnetic and clastic content with coarser overall magnetic and clastic grain size and are likely intervals of enhanced rainfall and runoff from the NE South American margin to the coastal ocean. In contrast, intervals B, D, F, and H have lower clastic flux with finer overall grain size, probably indicating lower continental rainfall and runoff. During the Holocene, high rainfall and runoff intervals can be related to cooler times and low rainfall and runoff to warmer times. The opposite pattern existed during the Pleistocene, with higher rainfall and runoff during interstadial conditions and lower rainfall and runoff during stadial conditions. We noted a similar pattern of Pleistocene multi-millennial-scale variability in a transect of deep-sea sediment cores along the NE Brazilian margin, from the Cariaco Basin (~10 N) to the NE Brazilian margin (~1° N–4° S). However the NW part of this transect (Cariaco Basin, Demerara Rise, Amazon Fan) has an out-of-phase relationship with the SE part of the transect (NE Brazilian margin) between warm–cold and wet–dry conditions. One possible cause of the high–low rainfall and runoff patterns might be oscillation of the Intertropical Convergence Zone (ITCZ), with higher rainfall and runoff associated with a more southerly average position of the ITCZ and lower rainfall and runoff associated with a more northerly average position of the ITCZ.

Using the Stable Isotopic Composition of Heliconoides inflatus Pteropod Shells to Determine Calcification Depth in the Cariaco Basin

Pteropods have been hailed as the “canary in the coal mine” for ocean acidification, however, questions remain about their life history, habitat, and the environmental parameters that the isotopic composition of their shells reflect. In order to use pteropods as recorders of ocean chemistry, it is first necessary to understand where they calcify and how this may change through the year, whether this signal is affected by dissolution, and if shells are retained in the subfossil, and eventually fossil, record. Here we create the first annual record of the stable isotopic composition of shells of the pteropod Heliconoides inflatus in the Cariaco Basin, Venezuela utilizing samples and data from the CARIACO time series. Sixty-four H. inflatus specimens from 17 sediment trap samples between November 1996 and April 1998, and 22 specimens from the late Holocene-aged CAR2000-MC-2 core were analyzed for shell condition (an assessment of the amount of dissolution that a shell has experienced), size, and carbon and oxygen isotopic composition. Carbon isotopic measurements of juveniles (< 1mm) were more variable than those in adults (>1 mm), suggesting juvenile pteropods likely have a higher growth rate, and therefore different metabolic vital effects, and a more varied diet than adult pteropods. H. inflatus was found to have an apparent calcification depth of 51.2 ± 34.0 m, suggesting they calcify at the shallowest part of their diurnal migration in the mixed layer (10–35 m in the Cariaco Basin). H. inflatus shell calcification will therefore only be impacted by changes in water chemistry at mixed layer depths. The shell condition did not impact the stable isotopic composition of the shells in either the sediment trap or core sample, suggesting the potential for using the isotopic composition of pteropod shells as oceanographic proxies when they are preserved. Comparisons between sediment trap and core sample show a 0.5°C warming that is marginally significant and a significant 0.45‰ decrease in δ13C between the late Holocene and the late 1990's. These measurements reflect changes in oceanic conditions linked to anthropogenic fossil fuel emissions known as the Suess effect, and lay the groundwork for establishing pteropods as paleoceanographic proxies in the future.

Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline

Little is known about viruses in oxygen-deficient water columns (ODWCs). In surface ocean waters, viruses are known to act as gene vectors among susceptible hosts. Some of these genes may have metabolic functions and are thus termed auxiliary metabolic genes (AMGs). AMGs introduced to new hosts by viruses can enhance viral replication and/or potentially affect biogeochemical cycles by modulating key microbial pathways. Here we identify 748 viral populations that cluster into 94 genera along a vertical geochemical gradient in the Cariaco Basin, a permanently stratified and euxinic ocean basin. The viral communities in this ODWC appear to be relatively novel as 80 of these viral genera contained no reference viral sequences, likely due to the isolation and unique features of this system. We identify viral elements that encode AMGs implicated in distinctive processes, such as sulfur cycling, acetate fermentation, signal transduction, [Fe–S] formation, and N-glycosylation. These AMG-encoding viruses include two putative Mu-like viruses, and viral-like regions that may constitute degraded prophages that have been modified by transposable elements. Our results provide an insight into the ecological and biogeochemical impact of viruses oxygen-depleted and euxinic habitats.

Updated Cariaco Basin 14C Calibration Dataset from 0–60 cal kyr BP

ABSTRACTWe present new updates to the calendar and radiocarbon (14C) chronologies for the Cariaco Basin, Venezuela. Calendar ages were generated by tuning abrupt climate shifts in Cariaco Basin sediments to those in speleothems from Hulu Cave. After the original Cariaco-Hulu calendar age model was published, Hulu Cave δ18O records have been augmented with increased temporal resolution and a greater number of U/Th dates. These updated Hulu Cave records provide increased accuracy as well as precision in the final Cariaco calendar age model. The depth scale for the Ocean Drilling Program Site 1002D sediment core, the primary source of samples for 14C dating, has been corrected to account for missing sediment from a core break, eliminating age-depth anomalies that afflicted the earlier calendar age models. Individual 14C dates for the Cariaco Basin remain unchanged from previous papers, although detailed comparisons of the Cariaco calibration dataset to those from Hulu Cave and Lake Suigetsu suggest that the Cariaco marine reservoir age may have shifted systematically during the past. We describe these recent changes to the Cariaco datasets and provide the data in a comprehensive format that will facilitate use by the community.

Determining how biotic and abiotic variables affect the shell condition and parameters of <i>Heliconoides inflatus</i> pteropods from a sediment trap in the Cariaco Basin

Pteropods have been nicknamed the “canary in the coal mine” for ocean acidification because they are predicted to be among the first organisms to be affected by changing ocean chemistry. This is due to their fragile, aragonitic shells and high abundances in polar and subpolar regions where the impacts of ocean acidification are most pronounced. For pteropods to be used most effectively as indicators of ocean acidification, the biotic and abiotic factors influencing their shell formation and dissolution in the modern ocean need to be quantified and understood. Here, we measured the shell condition (i.e., the degree to which a shell has dissolved) and shell characteristics, including size, number of whorls, shell thickness, and shell volume (i.e., amount of shell material) of nearly 50 specimens of the pteropod species Heliconoides inflatus sampled from a sediment trap in the Cariaco Basin, Venezuela, over an 11-month period. The shell condition of pteropods from sediment traps has the potential to be altered at three stages: (1) when the organisms are live in the water column associated with ocean acidification, (2) when organisms are dead in the water column associated with biotic decay of organic matter and/or abiotic dissolution associated with ocean acidification, and (3) when organisms are in the closed sediment trap cup associated with abiotic alteration by the preservation solution. Shell condition was assessed using two methods: the Limacina Dissolution Index (LDX) and the opacity method. The opacity method was found to capture changes in shell condition only in the early stages of dissolution, whereas the LDX recorded dissolution changes over a much larger range. Because the water in the Cariaco Basin is supersaturated with respect to aragonite year-round, we assume no dissolution occurred during life, and there is no evidence that shell condition deteriorated with the length of time in the sediment trap. Light microscope and scanning electron microscope (SEM) images show the majority of alteration happened to dead pteropods while in the water column associated with the decay of organic matter. The most altered shells occurred in samples collected in September and October when water temperatures were warmest and when the amount of organic matter degradation, both within the shells of dead specimens and in the water column, was likely to have been the greatest. The hydrographic and chemical properties of the Cariaco Basin vary seasonally due to the movement of the Intertropical Convergence Zone (ITCZ). Shells of H. inflatus varied in size, number of whorls, and thickness throughout the year. There was not a strong correlation between the number of whorls and the shell diameter, suggesting that shell growth is plastic. H. inflatus formed shells that were 40 % thicker and 20 % larger in diameter during nutrient-rich, upwelling times when food supply was abundant, indicating that shell growth in this aragonite-supersaturated basin is controlled by food availability. This study produces a baseline dataset of the variability in shell characteristics of H. inflatus pteropods in the Cariaco Basin and documents the controls on alteration of specimens captured via sediment traps. The methodology outlined for assessing shell parameters establishes a protocol for generating similar baseline records for pteropod populations globally.

Trace Element Heterogeneity Across Individual Planktic Foraminifera from the Modern Cariaco Basin

ABSTRACT The trace element composition of planktic foraminifera shells is influenced by both environmental and biological factors (‘vital effects’). As trace elements in individual foraminifera shells are increasingly used as paleoceanographic tools, understanding how trace element ratios vary between individuals, among species, and in response to high frequency environmental variability is of critical importance. Here, we present a three-year plankton tow record (2010–2012) of individual shell trace element (Mg, Sr, Ba, and Mn) to Ca ratios in the planktic species Globigerina ruber (pink), Orbulina universa, and Globorotalia menardii collected throughout the upper 100 m of Cariaco Basin. Plankton tows were paired with in situ measurements of water column chemistry and hydrography. The Mg/Ca ratio reflects different calcification temperatures in all three species when calculated using species-specific temperature relationships from single-species averages of Mg/Ca. However, individual shell Mg/Ca often results in unrealistic temperate estimates. The Sr/Ca ratios are relatively constant among the four species. Ratios of Mn/Ca and Ba/Ca are highest in G. menardii and are not reflective of elemental concentrations in open waters. The Mn/Ca ratio is elevated in all species during upwelling conditions, and a similar trend is demonstrated in Neogloboquadrina incompta shells from the California margin collected during upwelling periods. Together this suggests that elevated shell Mn/Ca may act as a tracer for upwelling of deeper water masses. Our results emphasize the large degree of trace element variability present among and within species living within a limited depth habitat and the roles of biology, calcification environment, and physical mixing in mediating how trace element geochemistry reflects environmental variability in the surface ocean.