Microbial ecosystem dynamics drive fluctuating nitrogen loss in marine anoxic zones.
Ontology highlight
ABSTRACT:
SUBMITTER: Penn JL
PROVIDER: S-EPMC6462081 | biostudies-literature | 2019 Apr
REPOSITORIES: biostudies-literature
Publications
Microbial ecosystem dynamics drive fluctuating nitrogen loss in marine anoxic zones.
Penn Justin L JL Weber Thomas T Chang Bonnie X BX Deutsch Curtis C
Proceedings of the National Academy of Sciences of the United States of America 20190325 15
The dynamics of nitrogen (N) loss in the ocean's oxygen-deficient zones (ODZs) are thought to be driven by climate impacts on ocean circulation and biological productivity. Here we analyze a data-constrained model of the microbial ecosystem in an ODZ and find that species interactions drive fluctuations in local- and regional-scale rates of N loss, even in the absence of climate variability. By consuming O<sub>2</sub> to nanomolar levels, aerobic nitrifying microbes cede their competitive advant ...[more]
Similar Datasets
Project description:Oxygen availability drives changes in microbial diversity and biogeochemical cycling between the aerobic surface layer and the anaerobic core in nitrite-rich anoxic marine zones (AMZs), which constitute huge oxygen-depleted regions in the tropical oceans. The current paradigm is that primary production and nitrification within the oxic surface layer fuel anaerobic processes in the anoxic core of AMZs, where 30-50% of global marine nitrogen loss takes place. Here we demonstrate that oxygenic photosynthesis in the secondary chlorophyll maximum (SCM) releases significant amounts of O2 to the otherwise anoxic environment. The SCM, commonly found within AMZs, was dominated by the picocyanobacteria Prochlorococcus spp. Free O2 levels in this layer were, however, undetectable by conventional techniques, reflecting a tight coupling between O2 production and consumption by aerobic processes under apparent anoxic conditions. Transcriptomic analysis of the microbial community in the seemingly anoxic SCM revealed the enhanced expression of genes for aerobic processes, such as nitrite oxidation. The rates of gross O2 production and carbon fixation in the SCM were found to be similar to those reported for nitrite oxidation, as well as for anaerobic dissimilatory nitrate reduction and sulfate reduction, suggesting a significant effect of local oxygenic photosynthesis on Pacific AMZ biogeochemical cycling.
| S-EPMC5547588 | biostudies-literature
Project description:Mechanistic description of the transition from aerobic to anaerobic metabolism is necessary for diagnostic and predictive modeling of fixed nitrogen loss in anoxic marine zones (AMZs). In a metabolic model where diverse oxygen- and nitrogen-cycling microbial metabolisms are described by underlying redox chemical reactions, we predict a transition from strictly aerobic to predominantly anaerobic regimes as the outcome of ecological interactions along an oxygen gradient, obviating the need for prescribed critical oxygen concentrations. Competing aerobic and anaerobic metabolisms can coexist in anoxic conditions whether these metabolisms represent obligate or facultative populations. In the coexistence regime, relative rates of aerobic and anaerobic activity are determined by the ratio of oxygen to electron donor supply. The model simulates key characteristics of AMZs, such as the accumulation of nitrite and the sustainability of anammox at higher oxygen concentrations than denitrification, and articulates how microbial biomass concentrations relate to associated water column transformation rates as a function of redox stoichiometry and energetics. Incorporating the metabolic model into an idealized two-dimensional ocean circulation results in a simulated AMZ, in which a secondary chlorophyll maximum emerges from oxygen-limited grazing, and where vertical mixing and dispersal in the oxycline also contribute to metabolic co-occurrence. The modeling approach is mechanistic yet computationally economical and suitable for global change applications.
| S-EPMC6908664 | biostudies-literature
Project description:Iron (Fe) and copper (Cu) are essential cofactors for microbial metalloenzymes, but little is known about the metalloenyzme inventory of anaerobic marine microbial communities despite their importance to the nitrogen cycle. We compared dissolved O2, NO[Formula: see text], NO[Formula: see text], Fe and Cu concentrations with nucleic acid sequences encoding Fe and Cu-binding proteins in 21 metagenomes and 9 metatranscriptomes from Eastern Tropical North and South Pacific oxygen minimum zones and 7 metagenomes from the Bermuda Atlantic Time-series Station. Dissolved Fe concentrations increased sharply at upper oxic-anoxic transition zones, with the highest Fe:Cu molar ratio (1.8) occurring at the anoxic core of the Eastern Tropical North Pacific oxygen minimum zone and matching the predicted maximum ratio based on data from diverse ocean sites. The relative abundance of genes encoding Fe-binding proteins was negatively correlated with O2, driven by significant increases in genes encoding Fe-proteins involved in dissimilatory nitrogen metabolisms under anoxia. Transcripts encoding cytochrome c oxidase, the Fe- and Cu-containing terminal reductase in aerobic respiration, were positively correlated with O2 content. A comparison of the taxonomy of genes encoding Fe- and Cu-binding vs. bulk proteins in OMZs revealed that Planctomycetes represented a higher percentage of Fe genes while Thaumarchaeota represented a higher percentage of Cu genes, particularly at oxyclines. These results are broadly consistent with higher relative abundance of genes encoding Fe-proteins in the genome of a marine planctomycete vs. higher relative abundance of genes encoding Cu-proteins in the genome of a marine thaumarchaeote. These findings highlight the importance of metalloenzymes for microbial processes in oxygen minimum zones and suggest preferential Cu use in oxic habitats with Cu > Fe vs. preferential Fe use in anoxic niches with Fe > Cu.
| S-EPMC4585252 | biostudies-literature
Project description:Dissolved oxygen (DO) concentrations shape the biogeochemistry and ecological structure of aquatic ecosystems; as a result, understanding how and why DO varies in space and time is of fundamental importance. Using high-resolution, in situ DO time-series collected over the course of a year in a novel marine ecosystem (Jellyfish Lake, Palau), we show that DO declined throughout the marine lake and subsequently recovered in the upper water column. These shifts were accompanied by variations in water temperature and were correlated to changes in wind, precipitation, and especially sea surface height that occurred during the 2015-2016 El Niño-Southern Oscillation event. Multiple approaches used to calculate rates of community respiration, net community production, and gross primary production from DO changes showed that DO consumption and production did not accelerate nor collapse; instead, their variance increased during lake deoxygenation and recovery, and then stabilized. Spatial and temporal variations in rates were significantly related to climatic variability and changes in DO, and causality testing indicated that these relationships were both correlative and causative. Our data indicate that climatic, physical, and biogeochemical properties and processes collectively regulated DO, producing linked feedbacks that drove DO decline and recovery.
| S-EPMC6834605 | biostudies-literature
Project description:The granular sludge process is an effective, low-footprint alternative to conventional activated sludge wastewater treatment. The architecture of the microbial granules allows the co-existence of different functional groups, e.g., nitrifying and denitrifying communities, which permits compact reactor design. However, little is known about the factors influencing community assembly in granular sludge, such as the effects of reactor operation strategies and influent wastewater composition. Here, we analyze the development of the microbiomes in parallel laboratory-scale anoxic/aerobic granular sludge reactors operated at low (0.9 kg m-3d-1), moderate (1.9 kg m-3d-1) and high (3.7 kg m-3d-1) organic loading rates (OLRs) and the same ammonium loading rate (0.2 kg NH4-N m-3d-1) for 84 days. Complete removal of organic carbon and ammonium was achieved in all three reactors after start-up, while the nitrogen removal (denitrification) efficiency increased with the OLR: 0% at low, 38% at moderate, and 66% at high loading rate. The bacterial communities at different loading rates diverged rapidly after start-up and showed less than 50% similarity after 6 days, and below 40% similarity after 84 days. The three reactor microbiomes were dominated by different genera (mainly Meganema, Thauera, Paracoccus, and Zoogloea), but these genera have similar ecosystem functions of EPS production, denitrification and polyhydroxyalkanoate (PHA) storage. Many less abundant but persistent taxa were also detected within these functional groups. The bacterial communities were functionally redundant irrespective of the loading rate applied. At steady-state reactor operation, the identity of the core community members was rather stable, but their relative abundances changed considerably over time. Furthermore, nitrifying bacteria were low in relative abundance and diversity in all reactors, despite their large contribution to nitrogen turnover. The results suggest that the OLR has considerable impact on the composition of the granular sludge communities, but also that the granule communities can be dynamic even at steady-state reactor operation due to high functional redundancy of several key guilds. Knowledge about microbial diversity with specific functional guilds under different operating conditions can be important for engineers to predict the stability of reactor functions during the start-up and continued reactor operation.
| S-EPMC5410608 | biostudies-literature
Project description:Fungi contribute extensively to a wide range of ecosystem processes, including decomposition of organic carbon, deposition of recalcitrant carbon, and transformations of nitrogen and phosphorus. In this review, we discuss the current knowledge about physiological and morphological traits of fungi that directly influence these processes, and we describe the functional genes that encode these traits. In addition, we synthesize information from 157 whole fungal genomes in order to determine relationships among selected functional genes within fungal taxa. Ecosystem-related traits varied most at relatively coarse taxonomic levels. For example, we found that the maximum amount of variance for traits associated with carbon mineralization, nitrogen and phosphorus cycling, and stress tolerance could be explained at the levels of order to phylum. Moreover, suites of traits tended to co-occur within taxa. Specifically, the genetic capacities for traits that improve stress tolerance-?-glucan synthesis, trehalose production, and cold-induced RNA helicases-were positively related to one another, and they were more evident in yeasts. Traits that regulate the decomposition of complex organic matter-lignin peroxidases, cellobiohydrolases, and crystalline cellulases-were also positively related, but they were more strongly associated with free-living filamentous fungi. Altogether, these relationships provide evidence for two functional groups: stress tolerators, which may contribute to soil carbon accumulation via the production of recalcitrant compounds; and decomposers, which may reduce soil carbon stocks. It is possible that ecosystem functions, such as soil carbon storage, may be mediated by shifts in the fungal community between stress tolerators and decomposers in response to environmental changes, such as drought and warming.
| S-EPMC4429240 | biostudies-literature
Project description:Nitrite is a pivotal component of the marine nitrogen cycle. The fate of nitrite determines the loss or retention of fixed nitrogen, an essential nutrient for all organisms. Loss occurs via anaerobic nitrite reduction to gases during denitrification and anammox, while retention occurs via nitrite oxidation to nitrate. Nitrite oxidation is usually represented in biogeochemical models by one kinetic parameter and one oxygen threshold, below which nitrite oxidation is set to zero. Here we find that the responses of nitrite oxidation to nitrite and oxygen concentrations vary along a redox gradient in a Pacific Ocean oxygen minimum zone, indicating niche differentiation of nitrite-oxidizing assemblages. Notably, we observe the full inhibition of nitrite oxidation by oxygen addition and nitrite oxidation coupled with nitrogen loss in the absence of oxygen consumption in samples collected from anoxic waters. Nitrite-oxidizing bacteria, including novel clades with high relative abundance in anoxic depths, were also detected in the same samples. Mechanisms corresponding to niche differentiation of nitrite-oxidizing bacteria across the redox gradient are considered. Implementing these mechanisms in biogeochemical models has a significant effect on the estimated fixed nitrogen budget.
| S-EPMC8114937 | biostudies-literature
Project description:Intertidal systems are complex and dynamic environments with many interacting factors influencing biochemical characteristics and microbial communities. One key factor are the actions of resident fauna, many of which are regarded as ecosystem engineers because of their bioturbation, bioirrigation and sediment stabilising activities. The purpose of this investigation was to elucidate the evolutionary implications of the ecosystem engineering process by identifying, if any, aspects that act as selection pressures upon microbial communities. A mesocosm study was performed using the well characterised intertidal ecosystem engineers Corophium volutator, Hediste diversicolor, and microphytobenthos, in addition to manual turbation of sediments to compare effects of bioturbation, bioirrigation and stabilisation. A range of sediment functions and biogeochemical gradients were measured in conjunction with 16S rRNA sequencing and diatom taxonomy, with downstream bacterial metagenome function prediction, to identify selection pressures that incited change to microbial community composition and function. Bacterial communities were predominantly Proteobacteria, with the relative abundance of Bacteroidetes, Alphaproteobacteria and Verrucomicrobia being partially displaced by Deltaproteobacteria, Acidobacteria and Chloroflexi as dissolved oxygen concentration and redox potential decreased. Bacterial community composition was driven strongly by biogeochemistry; surface communities were affected by a combination of sediment functions and overlying water turbidity, and subsurface communities by biogeochemical gradients driven by sediment reworking. Diatom communities were dominated by Nitzschia laevis and Achnanthes sp., and assemblage composition was influenced by overlying water turbidity (manual or biogenic) rather than direct infaunal influences such as grazing.
| S-EPMC7895378 | biostudies-literature
Project description:Trophic interactions can result in changes to the abundance and distribution of habitat-forming species that dramatically reduce ecosystem functioning. In the coastal zone of the Aleutian Archipelago, overgrazing by herbivorous sea urchins that began in the 1990s resulted in widespread deforestation of the region's kelp forests, which led to lower macroalgal abundances and higher benthic irradiances. We examined how this deforestation impacted ecosystem function by comparing patterns of net ecosystem production (NEP), gross primary production (GPP), ecosystem respiration (Re), and the range between GPP and Re in remnant kelp forests, urchin barrens, and habitats that were in transition between the two habitat types at nine islands that spanned more than 1000 kilometers of the archipelago. Our results show that deforestation, on average, resulted in a 24% reduction in GPP, a 26% reduction in Re, and a 24% reduction in the range between GPP and Re. Further, the transition habitats were intermediate to the kelp forests and urchin barrens for these metrics. These opposing metabolic processes remained in balance; however, which resulted in little-to-no changes to NEP. These effects of deforestation on ecosystem productivity, however, were highly variable between years and among the study islands. In light of the worldwide declines in kelp forests observed in recent decades, our findings suggest that marine deforestation profoundly affects how coastal ecosystems function.
| S-EPMC7055868 | biostudies-literature
Project description:Since 1960, landings of Atlantic herring have been the greatest of any marine species in Canada, surpassing Atlantic cod and accounting for 24% of the total seafood harvested in Atlantic Canada. The Scotian Shelf-Bay of Fundy herring fisheries (NAFO Division 4VWX) is among Canada's oldest and drives this productivity, accounting for up to 75% of the total herring catch in some years. The stocks' productivity and overall health have declined since 1965. Despite management measures to promote recovery implemented since 2003, biomass remains low and is declining. The factors that drive the productivity of 4VWX herring are primarily unresolved, likely impeding the effectiveness of management actions on this stock. We evaluated potential drivers of herring variability by analyzing 52 time-series that describe the temporal and spatial evolution of the 4VWX herring population and the physical, ecological, and anthropogenic factors that could affect them using structural equation models. Variation in herring biomass was best accounted for by the exploitation rate's negative effect and the geographic distribution of fishing and recruitment. Thermal phenology and temperature adversely and egg predation positively impacted the early life stage mortality rate and, ultimately, adult biomass. These findings are broadly relevant to fisheries management, but particularly for 4VWX herring, where the current management approach does not consider their early life stage dynamics or assess them within the ecosystem or climate change contexts.
| S-EPMC8717267 | biostudies-literature