skip to main content

Title: Nitrate respiration and diel migration patterns of diatoms are linked in sediments underneath a microbial mat

Diatoms are among the few eukaryotes known to store nitrate (NO3) and to use it as an electron acceptor for respiration in the absence of light and O2. Using microscopy and15N stable isotope incubations, we studied the relationship between dissimilatory nitrate/nitrite reduction to ammonium (DNRA) and diel vertical migration of diatoms in phototrophic microbial mats and the underlying sediment of a sinkhole in Lake Huron (USA). We found that the diatoms rapidly accumulated NO3at the mat‐water interface in the afternoon and 40% of the population migrated deep into the sediment, where they were exposed to dark and anoxic conditions for ~75% of the day. The vertical distribution of DNRA rates and diatom abundance maxima coincided, suggesting that DNRA was the main energy generating metabolism of the diatom population. We conclude that the illuminated redox‐dynamic ecosystem selects for migratory diatoms that can store nitrate for respiration in the absence of light. A major implication of this study is that the dominance of DNRA over denitrification is not explained by kinetics or thermodynamics. Rather, the dynamic conditions select for migratory diatoms that perform DNRA and can outcompete sessile denitrifiers.

 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  
Award ID(s):
Publication Date:
Journal Name:
Environmental Microbiology
Page Range or eLocation-ID:
p. 1422-1435
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    While inundated, small ponds (< 1000 m2area) account for disproportionately large contributions of CO2efflux to the global carbon budget and also store carbon in anoxic sediments. However, pond hydrology is shifting toward increasingly dry conditions in alpine and temperate zones, which might lead to increased exposure of shallow pond sediments. We analyzed sediment CO2efflux rates in dried sediments of multiple ponds of varying hydrology and sediment characteristics at montane and subalpine elevations near the Rocky Mountain Biological Laboratory in Colorado. Average CO2efflux rates from exposed sediments, 331.5 ± 11.5 mmol m−2d−1at the montane sites and 142.8 ± 45.1 mmol m−2d−1at the subalpine sites, were 10 times higher than average CO2efflux rates from pond water. Principal components analysis to reduce dimensionality of sediment characteristics revealed that random inter‐pond differences rather than exposure timing or hydroperiod drove variation among sediments. In linear mixed effects models of CO2flux rates, significant predictors included sediment moisture and temperature, pH, total organic carbon, and organic matter content at all pond hydroperiod classifications and sites. However, the sediment characteristics explaining the most variance differed among sites and hydroperiods and included nitrate concentrations, pH, bulk density, and temperature. We conclude that pond sediments are heterogeneous both within and among ponds in close proximity, and drivers of relativelymore »high CO2efflux rates differ among pond hydroperiods and elevations. This work emphasizes that local differences can impact predictions of CO2flux from lentic sediments which are becoming increasingly exposed.

    « less
  2. Abstract

    The enzyme carbonic anhydrase (CA) is crucial to many physiological processes involvingCO2, from photosynthesis and respiration, to calcification andCaCO3dissolution. We present new measurements of CA activity along a North Pacific transect, on samples from in situ pumps, sediment traps, discreet plankton samples from the ship's underway seawater line, plankton tows, and surface sediment samples from multicores. CA activity is highest in the surface ocean and decreases with depth, both in suspended and sinking particles. Subpolar gyre surface particles exhibit 10× higher CA activity per liter of seawater compared to subtropical gyre surface particles. Activity persists to 4700 m in the subpolar gyre, but only to 1000 m in the subtropics. All sinking CA activity normalized to particulate organic carbon (POC) follows a single relationship (CA/POC = 1.9 ± 0.2 × 10−7mol mol−1). This relationship is consistent with CA/POC values in subpolar plankton tow material, suspended particles, and core top sediments. We hypothesize that most subpolar CA activity is associated with rapidly sinking diatom blooms, consistent with a large mat of diatomaceous material identified on the seafloor. Compared to the basin‐wide sinking CA/POC relationship, a lower subtropical CA/POC suggests that the inventory of subtropical biomass is different in composition from exported material. Pteropods also demonstrate substantial CAmore »activity. Scaled to the volume within pteropod shells, first‐orderCO2hydration rate constants are elevated ≥ 1000× above background. This kinetic enhancement is large enough to catalyze carbonate dissolution within microenvironments, providing observational evidence for CA‐catalyzed, respiration‐drivenCaCO3dissolution in the shallow North Pacific.

    « less
  3. Huber, Julie A. (Ed.)
    ABSTRACT Wind-driven upwelling followed by relaxation results in cycles of cold nutrient-rich water fueling intense phytoplankton blooms followed by nutrient depletion, bloom decline, and sinking of cells. Surviving cells at depth can then be vertically transported back to the surface with upwelled waters to seed another bloom. As a result of these cycles, phytoplankton communities in upwelling regions are transported through a wide range of light and nutrient conditions. Diatoms appear to be well suited for these cycles, but their responses to them remain understudied. To investigate the bases for diatoms’ ecological success in upwelling environments, we employed laboratory simulations of a complete upwelling cycle with a common diatom, Chaetoceros decipiens , and coccolithophore, Emiliania huxleyi . We show that while both organisms exhibited physiological and transcriptomic plasticity, the diatom displayed a distinct response enabling it to rapidly shift-up growth rates and nitrate assimilation when returned to light and available nutrients following dark nutrient-deplete conditions. As observed in natural diatom communities, C. decipiens highly expresses before upwelling, or frontloads, key transcriptional and nitrate assimilation genes, coordinating its rapid response to upwelling conditions. Low-iron simulations showed that C. decipiens is capable of maintaining this response when iron is limiting to growth,more »whereas E. huxleyi is not. Differential expression between iron treatments further revealed specific genes used by each organism under low iron availability. Overall, these results highlight the responses of two dominant phytoplankton groups to upwelling cycles, providing insight into the mechanisms fueling diatom blooms during upwelling events. IMPORTANCE Coastal upwelling regions are among the most biologically productive ecosystems. During upwelling events, nutrient-rich water is delivered from depth resulting in intense phytoplankton blooms typically dominated by diatoms. Along with nutrients, phytoplankton may also be transported from depth to seed these blooms then return to depth as upwelling subsides creating a cycle with varied conditions. To investigate diatoms’ success in upwelling regions, we compare the responses of a common diatom and coccolithophore throughout simulated upwelling cycles under iron-replete and iron-limiting conditions. The diatom exhibited a distinct rapid response to upwelling irrespective of iron status, whereas the coccolithophore’s response was either delayed or suppressed depending on iron availability. Concurrently, the diatom highly expresses, or frontloads, nitrate assimilation genes prior to upwelling, potentially enabling this rapid response. These results provide insight into the molecular mechanisms underlying diatom blooms and ecological success in upwelling regions.« less
  4. Abstract

    Temperature and nutrients are fundamental, highly nonlinear drivers of biological processes, but we know little about how they interact to influence growth. This has hampered attempts to model population growth and competition in dynamic environments, which is critical in forecasting species distributions, as well as the diversity and productivity of communities. To address this, we propose a model of population growth that includes a new formulation of the temperature–nutrient interaction and test a novel prediction: that a species’ optimum temperature for growth,Topt, is a saturating function of nutrient concentration. We find strong support for this prediction in experiments with a marine diatom,Thalassiosira pseudonana:Toptdecreases by 3–6 °C at low nitrogen and phosphorus concentrations. This interaction implies that species are more vulnerable to hot, low‐nutrient conditions than previous models accounted for. Consequently the interaction dramatically alters species’ range limits in the ocean, projected based on current temperature and nitrate levels as well as those forecast for the future. Ranges are smaller not only than projections based on the individual variables, but also than those using a simpler model of temperature–nutrient interactions. Nutrient deprivation is therefore likely to exacerbate environmental warming's effects on communities.

  5. Subsurface chlorophyll maximum layers (SCMLs) are nearly ubiquitous in stratified water columns and exist at horizontal scales ranging from the submesoscale to the extent of oligotrophic gyres. These layers of heightened chlorophyll and/or phytoplankton concentrations are generally thought to be a consequence of a balance between light energy from above and a limiting nutrient flux from below, typically nitrate (NO3). Here we present multiple lines of evidence demonstrating that iron (Fe) limits or with light colimits phytoplankton communities in SCMLs along a primary productivity gradient from coastal to oligotrophic offshore waters in the southern California Current ecosystem. SCML phytoplankton responded markedly to added Fe or Fe/light in experimental incubations and transcripts of diatom and picoeukaryote Fe stress genes were strikingly abundant in SCML metatranscriptomes. Using a biogeochemical proxy with data from a 40-y time series, we find that diatoms growing in California Current SCMLs are persistently Fe deficient during the spring and summer growing season. We also find that the spatial extent of Fe deficiency within California Current SCMLs has significantly increased over the last 25 y in line with a regional climate index. Finally, we show that diatom Fe deficiency may be common in the subsurface of major upwellingmore »zones worldwide. Our results have important implications for our understanding of the biogeochemical consequences of marine SCML formation and maintenance.

    « less