Biology subjects

Babbin, A. R.

Publications and source records attributed to Babbin, A. R..

10 recordsLinked to original sources

bioRxiv2024

Ecological dynamics explain modular denitrification in the ocean

Microorganisms in marine oxygen minimum zones (OMZs) drive globally impactful biogeochemical processes. One such process is the multi-step denitrification, the dominant pathway for 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 only subsets ("modules") of the complete pathway. Here, we identify the ecological mechanisms sustaining diverse denitrifiers, explain the observed 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 growth is limited by organic matter (OM), explaining the viability of populations respiring nitrite and N2O in a nitrate-filled ocean. Results predict denitrifier community succession along environmental gradients: shorter versus longer modules are favored when OM versus N limits growth, respectively, suggesting a niche for the NO3-{longrightarrow}NO2- module in free-living communities and for the complete pathway in organic particles, consistent with observations. The model captures and mechanistically explains the observed dominance and higher oxygen tolerance of the NO3-{longrightarrow}NO2- module. Results also capture observations that nitrate is the dominant source of N2O. These results advance the mechanistic understanding of the relationship between microbial ecology and N loss, which is essential for accurately predicting the oceans future.

ecology↗

bioRxiv2023

Origin, age, and metabolisms of dominant anammox bacteria in the global oxygen deficient zones

Anammox bacteria inhabiting oxygen deficient zones (ODZs) are a major functional group mediating fixed nitrogen loss and thus exerting a critical control on the nitrogen budget in the global ocean. However, the diversity, origin, and broad metabolisms of ODZ anammox bacteria remain unknown. Here we report two novel metagenome-assembled genomes of Scalindua, which represent most, if not all, of the anammox bacteria in the global ODZs. Beyond the core anammox metabolism, both organisms contain cyanase and the more dominant one encodes a urease, indicating ODZ anammox bacteria can utilize cyanate and urea in addition to ammonium. The first ODZ Scalindua likely derived from the benthos [~]200 million years ago. Compared to benthic strains of the same clade, ODZ Scalindua uniquely encode genes for urea utilization but lost genes related to growth arrest, flagellum synthesis, and chemotaxis, presumably for adaptation to the anoxic water column.

microbiology↗

bioRxiv2023

Uncultivated DPANN archaea are ubiquitous inhabitants of global oxygen deficient zones with diverse metabolic potential

Archaea belonging to the DPANN superphylum have been found within 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 15-26% 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 belonging to DPANN phyla Nanoarchaeota, Pacearchaeota, Woesarchaeota, Undinarchaeota, Iainarchaeota, and SpSt-1190 from pelagic ODZs in the Eastern Tropical North Pacific and Arabian Sea. We find these archaea to be permanent, stable residents of all 3 major ODZs only within anoxic depths, comprising up to 1% of the total microbial community and up to 25-50% of archaea. ODZ DPANN appear 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 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 3 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.

microbiology↗

bioRxiv2023

A new abundant nitrite-oxidizing phylum in oligotrophic marine sediments

Nitrite-oxidizing bacteria (NOB) are important nitrifiers whose activity regulates the availability of nitrite and links reduced ammonium and oxidized nitrate in ecosystems. In oxic marine sediments, ammonia-oxidizing archaea (AOA) and NOB together catalyze the oxidation of ammonium to nitrate, but the observed abundance ratios of AOA to canonical NOB are significantly higher than the theoretical ratio predicted from microbial physiology, indicating that many novel NOBs are yet to be discovered. Here we report a new bacterial phylum Candidatus Nitrosediminicolota, 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 aerophilis) is generally confined within the oxic zone, another (Ca. Nitrosediminicola anaerotolerans) can additionally thrive in anoxic sediments. Counting Ca. Nitrosediminicolota as a nitrite-oxidizer resolves the apparent abundance imbalance between AOA and NOB in oxic marine sediments, and thus its activity may exert a critical control on the nitrite budget.

microbiology↗

bioRxiv2023

Physical structure and interstitial flows govern microbial life in microenvironments

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 versus diffusion, and even a modest flow through a pore in the range of 10 {micro}m s-1 can 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.

microbiology↗

bioRxiv2023

Genome-resolved metagenomics reveals abundant nitrate reducers and partitioning of nitrite usage within global oxygen deficient zones

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 steps, but many organisms possess only partial denitrification pathways, either producing or consuming key intermediates such as the greenhouse gas N2O. Marker gene surveys have revealed a diversity of denitrification genes within ODZs, but whether these genes are primarily carried by complete or partial denitrifiers and the identities of denitrifying taxa remain open questions. From 56 metagenomes spanning all three major ODZs, we use genome-resolved metagenomics 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 metagenome-assembled genomes presents the largest collection of pelagic ODZ microbes and reveals a clearer picture of the nitrogen cycling community within this environment.

microbiology↗

bioRxiv2022

Sinking diatom aggregates provide carbon to drive microscale denitrification in a bulk oxygenated ocean

Sinking marine particles drive the biological gravitational pump that naturally sequesters carbon dioxide from the atmosphere. Ubiquitous throughout the ocean, these particles are largely composed of phytoplankton that aggregate together or are repackaged by zooplankton into pellets that sink to the deep. Despite their small size, the compartmentalized nature of these particles promotes intense localized metabolic activity by the bacteria lucky enough to colonize them. Due to their sheer numbers, these microscale interactions can change the chemistry of the bulk ocean and impact global biogeochemical budgets. As soon as phytoplankton-derived particles are exported from the surface ocean, the fate of the carbon depends on the lability and availability of the carbon, the diffusive supply of oxidants from the bulk, and the development of microbial communities throughout the aggregate. Here we show with a model experimental system that aggregates composed of marine diatoms -- important primary producers substantially contributing to global carbon export -- can support active denitrification even among bulk oxygenated water ill-conducive to anaerobic metabolisms. We further show the primary nitrite maximum could be formed, in part, due to dissimilatory reduction of nitrate and nitrite occurring at anoxic microsites within such particles. Particle-based denitrification and other anaerobic metabolisms can change the global budget of elemental cycles important for life and climate across the oceans.

microbiology↗

bioRxiv2022

Nitrite accumulation and the associated anammox bacteria niche partitioning in marine sediments

By consuming ammonium and nitrite, anammox bacteria form an important functional guild in nitrogen cycling in many environments including marine sediments. Recent studies have shown that anammox bacteria can consume most of the upwardly diffusing ammonium from deep anoxic sediments; however, their impact on the other important substrate nitrite has not been well characterized. Here we show niche partitioning of two anammox families emerges in a 2.4-m long mostly anoxic sediment core retrieved from the Nordic Seas. We document high abundances (~106 cells g-1) of anammox bacteria in most investigated sediment layers, with two distinct anammox abundance maxima in two nitrite consumption zones. Between the two anammox abundance maxima, nitrite accumulates as observed in other marine sediment sites and aquatic environments, indicating anammox bacteria play a fundamental role in modulating the nitrite distribution. Anammox bacteria in the upper nitrite consumption zone are dominated by the Candidatus Bathyanammoxibiaceae family, while Ca. Scalinduaceae family dominate at the lower zone. A high-quality representative Ca. Bathyanammoxibiaceae genome is recovered, which, comparing to Ca. Scalindua sediminis, the representative of Scalinduaceae in marine sediments, has fewer high-affinity ammonium transporters and lacks the capacity to access alternative substrates or energy sources such as urea and cyanate. These features may restrict Ca. Bathyanammoxibiaceae to conditions of higher ammonium concentrations or fluxes, and therefore drive the observed niche partitioning. These findings improve our understanding about nitrogen cycling in marine sediments by revealing the association between nitrite accumulation and niche partitioning of anammox bacteria.

microbiology↗

bioRxiv2022

Porous marine snow differentially benefits chemotactic, motile, and non-motile bacteria

Particulate organic carbon settling through the marine water column is a key process that regulates 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 that bacterial motility is required for particle colonization and chemotaxis specifically benefits at higher settling velocities. We further explore the role of particle microstructure on the colonization efficiency of bacteria with different motility traits. We highlight that non-motile cells benefit disproportionally from the porous microstructure and are relatively enriched in the particle wake due to the efficient particle colonization of chemotactic and motile cells. Our results imply that although the chemotactic and motile bacteria benefit from the high nutrient availability when colonizing the particles, scavenging of these cells benefits the often oligotrophic, non-motile cells common among the planktonic community. Significance statementBacteria in the ocean rely on ephemeral nutrient patches from sinking marine particles, but attaching to these structures is challenging as particle settling rates often exceed bacterial swimming velocities and the numerically dominant marine bacteria are non-motile - posing an interesting paradox about the prominence of particle foraging. Here, we quantify the importance of chemotaxis and motility for the efficient colonization of marine particles and find that although chemotaxis provides a clear advantage, motility is the basic requirement for particle colonization. We expand this analysis to consider highly heterogeneous particle structures and find a disproportionate benefit for non-motile cells by facilitating a direct encounter with the particle surface and enriching non-motile microbes in the nutrient-rich particle plume.

microbiology↗

bioRxiv2021

Aerobic Bacteria Produce Nitric Oxide via Denitrification and Trigger Algal Population Collapse

Microbial interactions govern marine biogeochemistry. These interactions are generally considered to rely on exchange of organic molecules. Here we report on a novel inorganic route of microbial communication, showing that algal-bacterial interactions are mediated through inorganic nitrogen exchange. Under oxygen-rich conditions, aerobic bacteria reduce algal-secreted nitrite to nitric oxide (NO) through denitrification, a well-studied anaerobic respiration mechanism. Bacteria secrete NO, triggering a cascade in algae akin to programmed cell death. During death, algae further generate NO, thereby propagating the signal in the algal population. Eventually, the algal population collapses, similar to the sudden demise of oceanic algal blooms. Our study suggests that the exchange of denitrification intermediates, particularly in oxygenated environments, is an overlooked yet ecologically significant route of microbial communication within and across kingdoms. One Sentence SummaryAerobic bacteria activate denitrification in oxygenated conditions and produce nitric oxide that kills their algal partners

microbiology↗