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Abstract Nitrite is a ubiquitous compound found across aquatic systems and an intermediate in both the oxidative and reductive metabolisms transforming fixed nitrogen in the environment. Yet, the abiotic cycling of nitrite is often overlooked in favor of biologically mediated reactions. Here we quantify the apparent acid dissociation constant (pK_a) between nitrous acid and its conjugate base nitrite in both freshwater and seawater systems across a range of environmentally relevant temperatures (5–35°C) using potentiometric‐based titration. In freshwater, we measured a pK_a,NBSof 3.14 at 25°C and a pK_a,Tof 2.87 for seawater at the same temperature. We quantify substantial effects of both salinity and temperature on the pK_a, with colder and fresher water manifesting higher values and thus a greater proportion of protonated nitrite at any given pH. Because nitrous acid is unstable and decomposes to nitric oxide, the implications for the nitrous acid dissociation constant on ecosystem function are broad. 

ABSTRACT Most microbial life on Earth is found in localized microenvironments that collectively exert a crucial role in maintaining ecosystem health and influencing global biogeochemical cycles. In many habitats such as biofilms in aquatic systems, bacterial flocs in activated sludge, periphyton mats, or particles sinking in the ocean, these microenvironments experience sporadic or continuous flow. Depending on their microscale structure, pores and channels through the microenvironments permit localized flow that shifts the relative importance of diffusive and advective mass transport. How this flow alters nutrient supply, facilitates waste removal, drives the emergence of different microbial niches, and impacts the overall function of the microenvironments remains unclear. Here, we quantify how pores through microenvironments that permit flow can elevate nutrient supply to the resident bacterial community using a microfluidic experimental system and gain further insights from coupled population-based and computational fluid dynamics simulations. We find that the microscale structure determines the relative contribution of advection vs diffusion, and even a modest flow through a pore in the range of 10 µm s⁻¹can increase the carrying capacity of a microenvironment by 10%. Recognizing the fundamental role that microbial hotspots play in the Earth system, developing frameworks that predict how their heterogeneous morphology and potential interstitial flows change microbial function and collectively alter global scale fluxes is critical.IMPORTANCEMicrobial life is a key driver of global biogeochemical cycles. Similar to the distribution of humans on Earth, they are often not homogeneously distributed in nature but occur in dense clusters that resemble microbial cities. Within and around these clusters, diffusion is often assumed as the sole mass-transfer process that dictates nutrient supply and waste removal. In many natural and engineered systems such as biofilms in aquatic environments, aggregates in bioremediation, or flocs in wastewater treatment plants, these clusters are exposed to flow that elevates mass transfer, a process that is often overlooked. In this study, we show that advective fluxes can increase the local growth of bacteria in a single microenvironment by up to 50% and shape their metabolism by disrupting localized anoxia or supplying nutrients at different rates. Collectively, advection-enhanced mass transport may thus regulate important biogeochemical transformations in both natural and engineered environments. 

ABSTRACT Archaea belonging to the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota) superphylum have been found in an expanding number of environments and perform a variety of biogeochemical roles, including contributing to carbon, sulfur, and nitrogen cycling. Generally characterized by ultrasmall cell sizes and reduced genomes, DPANN archaea may form mutualistic, commensal, or parasitic interactions with various archaeal and bacterial hosts, influencing the ecology and functioning of microbial communities. While DPANN archaea reportedly comprise a sizeable fraction of the archaeal community within marine oxygen-deficient zone (ODZ) water columns, little is known about their metabolic capabilities in these ecosystems. We report 33 novel metagenome-assembled genomes (MAGs) belonging to the DPANN phyla Nanoarchaeota, Pacearchaeota, Woesearchaeota, Undinarchaeota, Iainarchaeota, and SpSt-1190 from pelagic ODZs in the Eastern Tropical North Pacific and the Arabian Sea. We find these archaea to be permanent, stable residents of all three major ODZs only within anoxic depths, comprising up to 1% of the total microbial community and up to 25%–50% of archaea as estimated from read mapping to MAGs. ODZ DPANN appear to be capable of diverse metabolic functions, including fermentation, organic carbon scavenging, and the cycling of sulfur, hydrogen, and methane. Within a majority of ODZ DPANN, we identify a gene homologous to nitrous oxide reductase. Modeling analyses indicate the feasibility of a nitrous oxide reduction metabolism for host-attached symbionts, and the small genome sizes and reduced metabolic capabilities of most DPANN MAGs suggest host-associated lifestyles within ODZs. IMPORTANCEArchaea from the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota) superphylum have diverse metabolic capabilities and participate in multiple biogeochemical cycles. While metagenomics and enrichments have revealed that many DPANN are characterized by ultrasmall genomes, few biosynthetic genes, and episymbiotic lifestyles, much remains unknown about their biology. We report 33 new DPANN metagenome-assembled genomes originating from the three global marine oxygen-deficient zones (ODZs), the first from these regions. We survey DPANN abundance and distribution within the ODZ water column, investigate their biosynthetic capabilities, and report potential roles in the cycling of organic carbon, methane, and nitrogen. We test the hypothesis that nitrous oxide reductases found within several ODZ DPANN genomes may enable ultrasmall episymbionts to serve as nitrous oxide consumers when attached to a host nitrous oxide producer. Our results indicate DPANN archaea as ubiquitous residents within the anoxic core of ODZs with the potential to produce or consume key compounds. 

Abstract Nitrite-oxidizing bacteria (NOB) are important nitrifiers whose activity regulates the availability of nitrite and dictates the magnitude of nitrogen loss in ecosystems. In oxic marine sediments, ammonia-oxidizing archaea (AOA) and NOB together catalyze the oxidation of ammonium to nitrate, but the abundance ratios of AOA to canonical NOB in some cores are significantly higher than the theoretical ratio range predicted from physiological traits of AOA and NOB characterized under realistic ocean conditions, indicating that some NOBs are yet to be discovered. Here we report a bacterial phylumCandidatusNitrosediminicolota, members of which are more abundant than canonical NOBs and are widespread across global oligotrophic sediments.Ca. Nitrosediminicolota members have the functional potential to oxidize nitrite, in addition to other accessory functions such as urea hydrolysis and thiosulfate reduction. While one recovered species (Ca. Nitrosediminicola aerophilus) is generally confined within the oxic zone, another (Ca. Nitrosediminicola anaerotolerans) additionally appears in anoxic sediments. CountingCa. Nitrosediminicolota as a nitrite-oxidizer helps to resolve the apparent abundance imbalance between AOA and NOB in oxic marine sediments, and thus its activity may exert controls on the nitrite budget. 

Abstract Anammox bacteria inhabiting oxygen-deficient zones (ODZs) are a major functional group mediating fixed nitrogen loss in the global ocean. However, many basic questions regarding the diversity, broad metabolisms, origin, and adaptive mechanisms of ODZ anammox bacteria remain unaddressed. Here we report two novel metagenome-assembled genomes of anammox bacteria affiliated with the Scalindua genus, which represent most, if not all, of the anammox bacteria in the global ODZs. Metagenomic read-recruiting and comparison with historical data show that they are ubiquitously present in all three major ODZs. Beyond the core anammox metabolism, both organisms contain cyanase, and the more dominant one encodes a urease, indicating most ODZ anammox bacteria can utilize cyanate and urea in addition to ammonium. Molecular clock analysis suggests that the evolutionary radiation of these bacteria into ODZs occurred no earlier than 310 million years ago, ~1 billion years after the emergence of the earliest modern-type ODZs. Different strains of the ODZ Scalindua species are also found in benthic sediments, and the first ODZ Scalindua is likely derived from the benthos. Compared to benthic strains of the same clade, ODZ Scalindua uniquely encodes genes for urea utilization but has lost genes related to growth arrest, flagellum synthesis, and chemotaxis, presumably for adaptation to thrive in the global ODZ waters. Our findings expand the known metabolisms and evolutionary history of the bacteria controlling the global nitrogen budget. 

Abstract Sinking marine particles drive the biological pump that naturally sequesters carbon from the atmosphere. Despite their small size, the compartmentalized nature of particles promotes intense localized metabolic activity by their bacterial colonizers. Yet the mechanisms promoting the onset of denitrification, a metabolism that arises once oxygen is limiting, remain to be established. Here we show experimentally that slow sinking aggregates composed of marine diatoms—important primary producers for global carbon export—support active denitrification even among bulk oxygenated water typically thought to exclude anaerobic metabolisms. Denitrification occurs at anoxic microsites distributed throughout a particle and within microns of a particle’s boundary, and fluorescence-reporting bacteria show nitrite can be released into the water column due to segregated dissimilatory reduction of nitrate and nitrite. Examining intact and broken diatoms as organic sources, we show slowly leaking cells promote more bacterial growth, allow particles to have lower oxygen, and generally support greater denitrification. 

Abstract Oxygen deficient zones (ODZs) account for about 30% of total oceanic fixed nitrogen loss via processes including denitrification, a microbially mediated pathway proceeding stepwise from NO3− to N2. This process may be performed entirely by complete denitrifiers capable of all four enzymatic steps, but many organisms possess only partial denitrification pathways, either producing or consuming key intermediates such as the greenhouse gas N2O. Metagenomics and marker gene surveys have revealed a diversity of denitrification genes within ODZs, but whether these genes co-occur within complete or partial denitrifiers and the identities of denitrifying taxa remain open questions. We assemble genomes from metagenomes spanning the ETNP and Arabian Sea, and map these metagenome-assembled genomes (MAGs) to 56 metagenomes from all three major ODZs to reveal the predominance of partial denitrifiers, particularly single-step denitrifiers. We find niche differentiation among nitrogen-cycling organisms, with communities performing each nitrogen transformation distinct in taxonomic identity and motility traits. Our collection of 962 MAGs presents the largest collection of pelagic ODZ microorganisms and reveals a clearer picture of the nitrogen cycling community within this environment. 

Abstract Particulate organic carbon settling through the marine water column is a key process that regulates the global climate by sequestering atmospheric carbon. The initial colonization of marine particles by heterotrophic bacteria represents the first step in recycling this carbon back to inorganic constituents—setting the magnitude of vertical carbon transport to the abyss. Here, we demonstrate experimentally using millifluidic devices that, although bacterial motility is essential for effective colonization of a particle leaking organic nutrients into the water column, chemotaxis specifically benefits at intermediate and higher settling velocities to navigate the particle boundary layer during the brief window of opportunity provided by a passing particle. We develop an individual-based model that simulates the encounter and attachment of bacterial cells with leaking marine particles to systematically evaluate the role of different parameters associated with bacterial run-and-tumble motility. We further use this model to explore the role of particle microstructure on the colonization efficiency of bacteria with different motility traits. We find that the porous microstructure facilitates additional colonization by chemotactic and motile bacteria, and fundamentally alters the way nonmotile cells interact with particles due to streamlines intersecting with the particle surface. 

Microorganisms in marine oxygen minimum zones (OMZs) drive globally impactful biogeochemical processes. One such process is multistep denitrification (NO₃^–→NO₂^–→NO→N₂O→N₂), which dominates OMZ bioavailable nitrogen (N) loss and nitrous oxide (N₂O) production. Denitrification-derived N loss is typically measured and modeled as a single step, but observations reveal that most denitrifiers in OMZs contain subsets (“modules”) of the complete pathway. Here, we identify the ecological mechanisms sustaining diverse denitrifiers, explain the prevalence of certain modules, and examine the implications for N loss. We describe microbial functional types carrying out diverse denitrification modules by their underlying redox chemistry, constraining their traits with thermodynamics and pathway length penalties, in an idealized OMZ ecosystem model. Biomass yields of single-step modules increase along the denitrification pathway when organic matter (OM) limits growth, which explains the viability of populations respiring NO₂^–and N₂O in a NO₃^–-filled ocean. Results predict denitrifier community succession along environmental gradients: Pathway length increases as the limiting substrate shifts from OM to N, suggesting a niche for the short NO₃^–→NO₂^–module in free-living, OM-limited communities, and for the complete pathway in organic particle-associated communities, consistent with observations. The model captures and mechanistically explains the observed dominance and higher oxygen tolerance of the NO₃^–→NO₂^–module. Results also capture observations that NO₃^–is the dominant source of N₂O. Our framework advances the mechanistic understanding of the relationship between microbial ecology and N loss in the ocean and can be extended to other processes and environments. 

Abstract By consuming ammonium and nitrite, anammox bacteria form an important functional guild in nitrogen cycling in many environments, including marine sediments. However, their distribution and impact on the important substrate nitrite has not been well characterized. Here we combined biogeochemical, microbiological, and genomic approaches to study anammox bacteria and other nitrogen cycling groups in two sediment cores retrieved from the Arctic Mid-Ocean Ridge (AMOR). We observed nitrite accumulation in these cores, a phenomenon also recorded at 28 other marine sediment sites and in analogous aquatic environments. The nitrite maximum coincides with reduced abundance of anammox bacteria. Anammox bacterial abundances were at least one order of magnitude higher than those of nitrite reducers and the anammox abundance maxima were detected in the layers above and below the nitrite maximum. Nitrite accumulation in the two AMOR cores co-occurs with a niche partitioning between two anammox bacterial families ( Candidatus Bathyanammoxibiaceae and Candidatus Scalinduaceae), likely dependent on ammonium availability. Through reconstructing and comparing the dominant anammox genomes ( Ca . Bathyanammoxibius amoris and Ca . Scalindua sediminis), we revealed that Ca . B. amoris has fewer high-affinity ammonium transporters than Ca . S. sediminis and lacks the capacity to access alternative substrates and/or energy sources such as urea and cyanate. These features may restrict Ca . Bathyanammoxibiaceae to conditions of higher ammonium concentrations. These findings improve our understanding about nitrogen cycling in marine sediments by revealing coincident nitrite accumulation and niche partitioning of anammox bacteria.