Biology subjects

Santoro, A. E.

Publications and source records attributed to Santoro, A. E..

11 recordsLinked to original sources

bioRxiv2024

Contribution of ammonia oxidizers to inorganic carbon fixation in the dark ocean

Ammonia-oxidizing archaea are the most abundant chemolithoautotrophs in the ocean, comprising up to 40% of microbial cells in deep waters, and are assumed to dominate dissolved inorganic carbon (DIC) fixation below the sunlit surface layer. Yet, the supply of reduced nitrogen from particulate organic matter flux from the surface is insufficient to support the amount of nitrification required to sustain measured DIC fixation rates in the dark ocean. The aim of this study was to quantify the contribution of ammonia oxidizers to DIC fixation in the dark ocean. We used phenylacetylene - a specific inhibitor of the ammonia monooxygenase enzyme - to selectively inhibit ammonia oxidizers during two oceanographic expeditions in the eastern tropical and subtropical Pacific Ocean spanning 35{o} N to 10{o} S. We show that ammonia oxidizers contribute only a small fraction to dark DIC fixation, accounting for 2 to 22% of the depth-integrated rates in the eastern tropical Pacific. The highest contributions were observed at the depth of the nitrification maximum, where ammonia oxidation could account for up to 50% of dark DIC fixation. Our results help to reconcile the observed discrepancies between nitrogen supply and DIC fixation at depth, and provide a new perspective on global ocean chemolithoautotrophy, revealing that the majority of DIC fixation within the lower euphotic zone and below 200 m depth is not fueled by ammonia oxidation. SignificanceMicrobes in the ocean play important roles in the global carbon cycle and the oceans capacity to sequester carbon. Despite this importance, deciphering the contributions of different microbial metabolic processes to the oceanic carbon budget remains challenging. Particularly in the dark ocean, large discrepancies between organic matter fluxes and measured microbial metabolic rates are observed. We show that abundant chemoautotrophs - ammonia-oxidizing microbes - contribute only a small fraction to dark carbon fixation in the Pacific Ocean, challenging the current view that carbon fixation in the dark ocean is primarily sustained by nitrification. This work advances our understanding of microbial carbon processing, and offers new insights into the long-standing question of the main energy sources fueling carbon fixation in the dark ocean.

microbiology↗

bioRxiv2024

Ocean carbon export can be predicted from ocean color-based phytoplankton communities

Carbon flux to the deep sea can be dictated by surface ocean phytoplankton community composition, but translating surface ocean observations into quantitative predictions of carbon export requires additional consideration of the underlying ecosystem drivers. Here, we used genetic tracers of phytoplankton detected in surface seawater and within sinking particles collected in the mesopelagic ocean to identify mechanistic links between surface communities and carbon export in the North Pacific and North Atlantic Oceans. Phytoplankton 18S rRNA sequences were sampled over a one-month period in surface seawater and within bulk-collected and individually-isolated sinking particles using mesopelagic sediment traps (100-500m). Nearly all phytoplankton amplicon sequence variants (ASVs) exported from the surface were packaged in large (>300 {micro}m) particles. Individually, these particles contained only a few distinct phytoplankton ASVs, but collectively, large particles transported about half of the surface taxonomic diversity into the mesopelagic. The relative sequence abundances of the surface community detected within particles were quantitatively related to measured POC fluxes: a linear model based on the relative sequence abundance of just two pigment-based phytoplankton taxa, diatoms and photosynthetic Hacrobia, was predictive of POC flux magnitude. These two taxa were also enriched within the ecologically-distinct particle classes that had the greatest influence on carbon export magnitude. As global, hyperspectral ocean color satellites begin to quantify these taxonomic groups in the surface ocean, the relationship of these taxa to carbon fluxes demonstrated here may help generate more accurate global estimates of export.

ecology↗

bioRxiv2024

Membrane permeability selection drove the stereochemistry of life

Early in the evolution of life a proto-metabolic network was encapsulated within a membrane compartment. The permeability characteristics of the membrane determined several key functions of this network by determining which compounds could enter the compartment and which compounds could not. One key feature of known life is the utilisation of right-handed D- ribose and deoxyribose sugars and left-handed L- amino acid stereochemical isomers (enantiomers), however, it is not clear why life adopted this specific chirality. We previously demonstrated that an archaeal and an intermediate membrane mimic, bearing a mixture of bacterial and archaeal lipid characteristics (a hybrid membrane), display increased permeability compared to bacterial-like membranes. Here, we investigate if these membranes can drive stereochemical selection on pentose sugars, hexose sugars and amino acids. Using permeability assays of homogenous unilamellar vesicles, we demonstrate that both membranes select for D- ribose and deoxyribose sugars while the hybrid membrane uniquely selects for a reduced alphabet of L- facing amino acids. This repertoire includes alanine, the plausible first L- amino acid utilised. We conclude such compartments could provide stereochemical compound selection thereby demonstrating a solution to the chirality problem during the evolution of life.

evolutionary biology↗

bioRxiv2023

Quantitative analysis of food web dynamics in a low export ecosystem

Food webs trace the flow of organic matter and energy among producers and consumers; for pelagic marine food webs, network complexity directly influences the amount and form of carbon exported to the deep ocean via the biological pump. Here we present a synoptic view of mixed layer food web dynamics observed during the late summer 2018 EXport Processes in the Ocean from Remote Sensing (EXPORTS) field campaign in the subarctic Northeast Pacific at the long-running time-series site, Ocean Station Papa. Carbon biomass reservoirs of phytoplankton, microzooplankton, and bacterioplankton, were approximately equal while mesozooplankton biomass was 70% lower. Live organisms composed [~]40% of the total particulate organic carbon within the mixed layer: the remainder was attributed to detritus. Rates of carbon transfer among reservoirs indicated production and assimilation rates were well balanced by losses, leaving little organic carbon available for export. The slight positive net community production rate generated organic carbon that was exported from the system in the form of food web byproducts, such as large fecal pellets generated by mesozooplankton. This characteristically regenerative food web had relatively slow turnover times with small-magnitude transfers of carbon relative to standing stocks that occurred amidst a high background concentration of detrital particles and dissolved organic matter. The concurrent estimation of food web components and rates revealed that separated processes dominated the transfer of carbon within the food web compared to those that contributed to export. Plain Language SummaryThe biological carbon pump drives a downward flux of organic matter from the sunlit surface ocean to the vast ocean interior. Ecological interactions in the surface ocean directly affect the amount and type of carbon that is exported to the deep ocean. In this study, we present a synthesis of the late summer mixed layer food web in the Northeast Pacific that was extensively characterized during the 2018 EXport Processes in the Ocean from Remote Sensing (EXPORTS) field campaign. We found the majority of carbon was recycled within the mixed layer by microbes through multiple transfers between producers and consumers. Larger organisms, mesozooplankton and salps, only consumed a small amount of carbon but through the formation of sinking fecal pellets were the main mechanism of transporting carbon out of the system. The study highlights the need to concurrently study microbial and large organism dynamics to develop a predictive understanding of the fate of organic carbon in the oceans. Key PointsO_LIThe microbial loop dominated carbon flow in the late summer mixed layer food web of the North Pacific, most net production was respired leaving little carbon available for export. C_LIO_LIActive production and consumption of organic carbon occurred amid a high background of detrital particulate organic carbon (58% of total) with slow turnover time, 66 d. C_LIO_LIMesozooplankton which had relatively minor carbon consumption rates created the majority of export production due to efficient repackaging of consumed material. C_LI

ecology↗

bioRxiv2023

Microbial siderophore production is tightly coupled to iron in hydrothermal plumes

Hydrothermal vents have emerged as an important source of iron to seawater, yet only a subset of iron is soluble and persists long enough to be available for surface biological uptake. The longevity and solubility of iron in seawater is governed by strong organic ligands, like siderophores, that are produced by marine microorganisms and are a part of the oceans dissolved iron-binding ligand pool. These ligands have been hypothesized to aid in the persistence of dissolved iron in hydrothermal environments. To explore this hypothesis, we measured iron, iron-binding ligands, and siderophores from 11 geochemically distinct sites along a 1,700 km section of the Mid-Atlantic Ridge. Siderophores were found in hydrothermal plumes at all sites, with proximity to the vent playing an important role in dictating siderophore types and diversity. The notable presence of amphiphilic siderophores may point to microbial utilization of siderophores to access particulate hydrothermal iron, and the exchange of dissolved and particulate iron. The tight coupling between strong ligands and dissolved iron within neutrally buoyant plumes across six distinct hydrothermal environments, and the presence of dissolved siderophores with siderophore-producing microbial genera, suggests that biological production of siderophores exerts a key control on hydrothermal dissolved iron concentrations.

biochemistry↗

bioRxiv2022

Synechococcus nitrogen gene loss in iron-limited ocean regions

Synechococcus are the most abundant cyanobacteria in high latitude regions and are responsible for an estimated 17% of annual marine primary productivity. Despite their biogeochemical importance, Synechococcus populations have been unevenly sampled across the ocean, with most studies focused on low-latitude strains. In particular, the near absence of Synechococcus genomes from high-latitude, High Nutrient Low Chlorophyll (HNLC) regions leaves a gap in our knowledge of picocyanobacterial adaptation to iron limitation and their influence on carbon, nitrogen, and iron cycles. We examined Synechococcus populations from the subarctic North Pacific, a well-characterized HNLC region, with quantitative metagenomics. Assembly with short and long reads produced two near complete Synechococcus metagenome-assembled genomes (MAGs). Quantitative metagenome-derived abundances of these populations matched well with flow cytometry counts, and the Synechococcus MAGs were estimated to comprise >99% of the Synechococcus at Station P. Whereas the Station P Synechococcus MAGs contained multiple genes for adaptation to iron limitation, both genomes lacked genes for uptake and assimilation of nitrate and nitrite, suggesting a dependence on ammonium, urea, and other forms of recycled nitrogen leading to reduced iron requirements. A global analysis of Synechococcus nitrate reductase abundance in the TARA Oceans dataset found nitrate assimilation genes are also lower in other HNLC regions. We propose nitrate and nitrite assimilation gene loss in Synechococcus represents an adaptation to severe iron limitation in high-latitude regions where ammonium availability is higher. Our findings have implications for models that quantify the contribution of cyanobacteria to primary production and subsequent carbon export. SignificanceThe cyanobacterium Synechococcus is a major contributor to ocean primary production and biogeochemistry. Here, we used quantitative metagenomics to assemble and enumerate two Synechococcus genomes from an iron-limited, High Nutrient Low Chlorophyll region. We show these genomes represent the majority of Synechococcus cells at the site and are the first known Synechococcus unable to assimilate either nitrate or nitrite. This gene loss is likely due to the high iron quota of these proteins and predominant availability of recycled forms of nitrogen. Synechococcus loss of nitrate assimilation affects their role in elemental cycles (e.g., carbon, nitrogen, and iron), limits their potential for carbon export, and enhances our understanding of Synechococcus evolution in response to nutrient limitation and competition.

ecology↗

bioRxiv2022

Carbon content, carbon fixation yield and dissolved organic carbon release from diverse marine nitrifiers

Nitrifying microorganisms, including ammonia-oxidizing archaea, ammonia-oxidizing bacteria and nitrite-oxidizing bacteria, are the most abundant chemoautotrophs in the ocean and play an important role in the global carbon cycle by fixing dissolved inorganic carbon (DIC) into biomass. The release of organic compounds by these microbes is less well known but may represent an as-yet unaccounted source of dissolved organic carbon (DOC) available to heterotrophic marine food webs. Here, we provide measurements of cellular carbon and nitrogen quotas, DIC fixation yields and DOC release of ten phylogenetically diverse marine nitrifiers grown in multiple culture conditions. All investigated strains released DOC during growth, making up on average 5-15% of the fixed DIC. Neither substrate concentration nor temperature affected the proportion of fixed DIC released as DOC, but release rates varied between closely related species. Our results also indicate previous studies may have underestimated DIC fixation yields of marine nitrite oxidizers due to partial decoupling of nitrite oxidation from CO2 fixation, and due to lower observed yields in artificial compared to natural seawater medium. The results of this study provide values for biogeochemical models of the global carbon cycle, and help to further constrain the implications of nitrification-fueled chemoautotrophy for marine food-web functioning and the biological sequestration of carbon in the ocean.

ecology↗

bioRxiv2020

Metabolic versatility of the nitrite-oxidizing bacterium Nitrospira marina and its proteomic response to oxygen-limited conditions

The genus Nitrospira is the most widespread group of chemolithoautotrophic nitrite-oxidizing bacteria that thrive in diverse natural and engineered ecosystems. Nitrospira marina Nb-295T represents the type genus and was isolated from the oceanic water column over 30 years ago, however, its genome has not yet been analyzed. Here, we analyzed the complete genome sequence of N. marina and performed select physiological experiments to test genome-derived hypotheses. Our data confirm that N. marina benefits from additions of undefined organic carbon substrates, has adaptations to combat oxidative, osmotic and UV-light induced stress and low dissolved pCO2, and is able to grow chemoorganotrophically on formate. We further investigated the metabolic response of N. marina to low (∼5.6 µM) O2 concentrations commonly encountered in marine environments with high nitrite concentrations. In response to O2-limited conditions, the abundance of a potentially more efficient CO2-fixing pyruvate:ferredoxin oxidoreductase (POR) complex and a high affinity cbb3-type terminal oxidase increased, suggesting a role in sustaining nitrite oxidation-driven autotrophy under O2 limitation. Additionally, a Cu/Zn-binding superoxide dismutase increased in abundance potentially protecting this putatively more O2-sensitive POR complex from oxidative damage. An increase in abundance of proteins involved in alternative energy metabolisms, including type 3b [NiFe] hydrogenase and formate dehydrogenase, indicate a high metabolic versatility to survive conditions unfavorable for aerobic nitrite oxidation. In summary, the genome and proteome of the first marine Nitrospira isolate identifies adaptations to life in the oxic ocean and provides important insights into the metabolic diversity and niche differentiation of NOB in marine environments.Competing Interest StatementThe authors have declared no competing interest.View Full Text

ecology↗

bioRxiv2020

Heterotrophic Thaumarchaeota with ultrasmall genomes are widespread in the ocean

The Thaumarchaeota comprise a diverse archaeal phylum including numerous lineages that play key roles in global biogeochemical cycling, particularly in the ocean. To date, all genomically-characterized marine Thaumarchaeota are reported to be chemolithoautotrophic ammonia-oxidizers. In this study, we report a group of heterotrophic marine Thaumarchaeota (HMT) with ultrasmall genome sizes that is globally abundant in deep ocean waters, apparently lacking the ability to oxidize ammonia. We assemble five HMT genomes from metagenomic data derived from both the Atlantic and Pacific Oceans, including two that are >95% complete, and show that they form a deeply-branching lineage sister to the ammonia-oxidizing archaea (AOA). Metagenomic read mapping demonstrates the presence of this group in mesopelagic samples from all major ocean basins, with abundances reaching up to 6% that of AOA. Surprisingly, the predicted sizes of complete HMT genomes are only 837-908 Kbp, and our ancestral state reconstruction indicates this lineage has undergone substantial genome reduction compared to other related archaea. The genomic repertoire of HMT indicates a highly reduced metabolism for aerobic heterotrophy that, although lacking the carbon fixation pathway typical of AOA, includes a divergent form III-a RuBisCO that potentially functions in a nucleotide scavenging pathway. Despite the small genome size of this group, we identify 13 encoded pyrroloquinoline quinone (PQQ)-dependent dehydrogenases that are predicted to shuttle reducing equivalents to the electron transport chain, suggesting these enzymes play an important role in the physiology of this group. Our results suggest that heterotrophic Thaumarchaeota are widespread in the ocean and potentially play key roles in global chemical transformations. ImportanceIt has been known for many years that marine Thaumarchaeota are abundant constituents of dark ocean microbial communities, where their ability to couple ammonia oxidation and carbon fixation plays a critical role in nutrient dynamics. In this study we describe an abundant group of heterotrophic marine Thaumarchaeota (HMT) in the ocean with physiology distinct from their ammonia-oxidizing relatives. HMT lack the ability to oxidize ammonia and fix carbon via the 3-hydroxypropionate/4-hydroxybutyrate pathway, but instead encode a form III-a RuBisCO and diverse PQQ-dependent dehydrogenases that are likely used to generate energy in the dark ocean. Our work expands the scope of known diversity of Thaumarchaeota in the ocean and provides important insight into a widespread marine lineage.

microbiology↗

bioRxiv2018

Phylogeny, evidence for a cryptic plastid, and distribution of Chytriodinium parasites (Dinophyceae) infecting copepods

Spores of the dinoflagellate Chytriodinium are known to infest copepod eggs causing their lethality. Despite the potential to control the population of such an ecologically important host, knowledge about Chytriodinium parasites is limited: we know little about phylogeny, parasitism, abundance, or geographical distribution. We carried out genome sequence surveys on four manually isolated sporocytes from the same sporangium to analyse the phylogenetic position of Chytriodinium based on SSU and concatenated SSU/LSU rRNA gene sequences, and also characterize two genes related to the plastidial heme pathway, hemL and hemY. The results suggest the presence of a cryptic plastid in Chytriodinium and a photosynthetic ancestral state of the parasitic Chytriodinium/Dissodinium clade. Finally, by mapping Tara Oceans V9 SSU amplicon data to the recovered SSU rRNA gene sequences from the sporocytes, we show that globally, Chytriodinium parasites are most abundant within the pico/nano- and mesoplankton of the surface ocean and almost absent within microplankton, a distribution indicating that they generally exist either as free-living spores or host-associated sporangia.

microbiology↗

bioRxiv2017

Correlated expression of archaeal ammonia oxidation machinery across disparate environmental and culture conditions

Thaumarchaea are ubiquitous in marine habitats where they participate in carbon and nitrogen cycling. Although metatranscriptomes suggest thaumarchaea are active microbes in marine waters, we understand little about how thaumarchaeal gene expression patterns relate to substrate utilization and activity. Here, we report the global transcriptional response of the marine ammonia-oxidizing thaumarchaeon Candidatus Nitrosopelagicus brevis str. CN25 to ammonia limitation using RNA-Seq. We further describe the genome and transcriptome of Ca. N. brevis str. U25, a new strain capable of urea utilization. Ammonia limitation in CN25 resulted in reduced expression of transcripts coding for ammonia oxidation proteins, and increased expression of a gene coding an Hsp20-like chaperone. Despite significantly different transcript abundances across treatments, two ammonia monooxygenase subunits (amoAB), a nitrite reductase (nirK), and both ammonium transporter genes were always among the most abundant transcripts, regardless of growth state. Ca. N. brevis str. U25 cells expressed a urea transporter 139-fold more than the urease catalytic subunit ureC. Gene co-expression networks derived from culture transcriptomes and ten thaumarchaea-enriched metatranscriptomes revealed a high degree of correlated gene expression across disparate environmental conditions and identified a module of genes, including amoABC and nirK, that we hypothesize to represent the core ammonia oxidation machinery.\n\nOriginality-Significance StatementDiscovering gene function in fastidious or uncultivated lineages remains one of the biggest challenges in environmental microbiology. Here, we use an approach that combines controlled laboratory experiments with in situ transcript abundance data from the environment to identify genes that share similar transcription patterns in marine ammonia-oxidizing thaumarchaea. These findings demonstrate how transcriptomes from microbial cultures can be used together with complex environmental samples to identify suites of co-expressed genes that are otherwise enigmatic and provide new insights into the mechanism of ammonia oxidation. Our results add to the growing body of literature showing that relatively small changes in transcript abundance are linked to large changes in growth in organisms with reduced genomes, suggesting they have limited capacity for metabolic regulation or that they rely on mechanisms other than transcriptional regulation to deal with a fluctuating environment.

microbiology↗