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Vallino, J. J.

Publications and source records attributed to Vallino, J. J..

8 recordsLinked to original sources

Aquatic bacterial metabolic rates from RNA quantitative stable isotope probing (RNA-qSIP) depend on experimental design

Quantitative stable isotope probing (qSIP) allows researchers to calculate taxon-specific carbon incorporation from sequencing of natural microbial communities, which can be used as a proxy for metabolic activity rates and subsequently as an input for biogeochemical modeling. While qSIP is widely utilized in soils to investigate the identity and metabolic activity of largely unculturable microbes, the application of qSIP in marine and aquatic ecosystems is more recent. Here, we investigated how bioreactor type (batch vs. chemostat) and carbon substrate complexity (single vs. multiple substrates) affect the incorporation of {superscript 1}3C-labeled glucose into rRNA after 24 hours using excess atomic fraction (EAF) as a proxy for metabolic activity rate. We found that the growth dynamics and community composition of the {superscript 1}3C-incorporating bacteria differed significantly for each treatment. EAF was positively correlated with both 16S gene copy number and a genomic index of copiotrophy in both batch treatments, but not in the chemostat, suggesting that chemostats dampen the competitive advantage of fast-growing copiotrophic taxa. Our results demonstrate that both substrate complexity and experimental regime influence qSIP-derived metabolic activity estimates and provide guidance for future applications of qSIP in aquatic environments.

molecular biology↗

Virus-mediated recycling of chemoautotrophic biomass

Aquatic environments absorb [~]2.5 gigatonnes of atmospheric carbon each year1, more than the carbon stored in the atmosphere, soils, and all biomass combined. Primary producers transform this dissolved inorganic carbon into biomass that can subsequently flow into other trophic levels, or be released back into the environment through viral lysis. While there is substantial knowledge about the diversity and activity of viruses infecting photoautotrophic primary producers, little is known about viruses infecting chemoautotrophs, representing a gap in our understanding of key microbial processes driving global carbon cycles. Here, we combine metagenomics with 12/13C stable isotopic probing mesocosm experiments in a marine-derived meromictic pond to quantify lineage-specific carbon cycling activity to identify key microbial populations driving carbon cycling. We then tracked the flow of carbon from active chemoautotrophs to their viruses and found evidence supporting virus-mediated recycling of chemoautotrophic biomass through the production of viral particles. In particular, active populations of hydrogen/sulfur-oxidizing chemoautotrophs (Thiomicrorhabdus, Hydrogenovibrio, Sulfurimonas, Sulfurovum) were targeted by viruses. Considering the widespread distribution of chemoautotrophs on Earth, we postulate that this previously overlooked component of the microbial carbon cycle is a globally relevant process that has implications for our planets carbon cycle. This work provides the foundation for revealing the role of viral lysis in chemoautotrophic primary production and builds toward biogeochemical models that incorporate viral recycling of chemoautotrophic biomass. Summary statementThe diversity, mechanisms, and processes governing microbial primary production and the recycling of autotrophic biomass are fundamental to our planets carbon cycle. These processes have implications for carbon sequestration, ocean biogeochemistry, and the overall balance of carbon dioxide in the atmosphere. Beneath the Earths sunlit layer, primary production is driven by microbial chemoautotrophs that derive energy from the oxidation of reduced compounds, such as hydrogen and sulfur, to form the base of the food web. Growing evidence suggests that aquatic ecosystems fueled by chemoautotrophy are widely distributed on Earth, ranging from beneath ice shelves to coastal upwelling regions to oxygen minimum zones, deep-sea hydrothermal vents and cold seeps, groundwater, and meromictic ponds and lakes2-7. Studying microbial processes regulating chemoautotrophic primary production and the recycling of chemoautotrophic biomass is fundamental to our understanding of global carbon cycles. While the diversity, function, and activity of viruses targeting photoautotrophs have been well-described across aquatic ecosystems8, we have little understanding of viruses involved in the recycling of chemoautotrophic biomass. Viruses are a major source of cellular mortality and carbon cycling in aquatic environments9-11. Viral lysis is estimated to transform [~]150 gigatonnes of carbon annually from biomass back into the environment, equivalent to [~]25 times that of the oceans biological carbon pump12,13. Despite recognition of the important role of viruses in aquatic habitats, there is a large gap in our understanding of the impact of viruses on globally distributed chemoautotrophs2,4,5,14-18. In this study, we show that viruses are not merely passive players but active agents recycling carbon fixed by productive chemoautotrophs, fundamentally reshaping how we view carbon and nutrient cycling in redox-active ecosystems.

microbiology↗

Deriving microbial food web structure by maximizing entropy production over variable timescales

Protists and viruses dynamically alter the flow of mass and energy through microbial food webs via predation. Simple microbial food web models show that the addition of microbial predators can increase the primary production of a microbial community but only for some configurations of food web structure. Under the conjecture that systems self-organize to maximize energy dissipation, known as the maximum entropy production (MEP) principle, we developed an MEP-based model that predicts microbial food web structure, and we examine how food web structure differs when entropy production is maximized over short versus long timescales. The model design follows from an experimental system and uses a trait-based variational method to set trait values by maximizing entropy production over a specified interval of time. Model results show that short-term MEP optimization (STO) produces microbial communities that specialize in substrate preference and consumers that have fewer trophic levels than solutions based on long-term optimization (LTO) that have substrate generalist and more trophic levels. Our MEP-based approach provides an alternative to food web structure synthesis that does not depend on assumptions of community stability.

microbiology↗

Metabolic and Population Profiles of Active Subseafloor Autotrophs in Young Oceanic Crust at Deep-Sea Hydrothermal Vents

At deep-sea hydrothermal vents, magmatically driven rock-water reactions in the crust generate gases and other reduced compounds that subseafloor microorganisms use for chemolithoautotrophy. In this study, microbial autotrophs from three diffuse flow hydrothermal vents at Axial Seamount in 2013 and 2014 were isotopically labeled using RNA Stable Isotope Probing (RNA-SIP), targeting subseafloor autotrophic mesophiles (30{degrees}C), thermophiles (55{degrees}C), and hyperthermophiles (80{degrees}C). We constructed taxonomic and functional profiles of active chemolithoautotrophs, examined population distributions across sites, and linked primary producers to their specific metabolic strategies within the subseafloor community. Dominant autotrophs exhibited hydrogen-dependent dissimilatory metabolisms such as sulfur and nitrate reduction and methanogenesis, as well as microaerophilic sulfide oxidation even at 80{degrees}C, consistent with fluid chemistries at each site. While hydrogenotrophic methanogenic archaea such as Methanothermococcus were restricted in their distribution and activity, hydrogenotrophic sulfur and nitrate reducers from the Aquificota (Thermovibrio), Campylobacterota (Nautiliaceae, Hydrogenimonas, and Desulfurobacteriaceae) were consistently active and present at all sites and years at both the population and community levels. Hydrogenase transcripts were significantly differentially expressed, and diverse hydrogenases were found in metagenome-assembled genomes of Aquificota members, highlighting the importance and versatility of their hydrogen utilization strategies which likely contribute to their cosmopolitan distribution across geochemically disparate subseafloor sites. Together, this study provides new insights into the functional dynamics and distribution of key subseafloor autotrophic microbial communities in young oceanic crust at deep-sea hydrothermal vents. IMPORTANCEDeep-sea hydrothermal vents are hotspots for life in the dark ocean, where rich animal ecosystems are supported by microbial primary producers utilizing the abundant chemical energy supplied by high-temperature water-rock reactions. Despite increasing knowledge about the geochemistry and microbiology of deep-sea hydrothermal vents, there is still a gap in our understanding of the key microbial players who fix much of the carbon at these sites, especially in the productive subseafloor. In this study, stable isotope probing was used to label active microbial autotrophs in diffuse flow venting fluids from three sites over two years and was combined with metatranscriptomic sequencing to identify their specific metabolic strategies. This research highlights the microbial community composition, function, gene regulation, and population dynamics that enable hydrothermal ecosystems to persist.

microbiology↗

Growth characteristics of natural microbial populations are skewed towards bacteria with low specific growth rates

Microbes are often functionally characterized by traits that specify their optimum environmental conditions for growth, such as temperature or pH, as well as upper and lower bounds where growth is possible. While any given microbe will have a narrow environmental window where growth can occur, a diverse community can span a much larger range of conditions where growth is possible by at least some members of the community. One important trait of microbes is maximum specific growth rate, as this trait determines if a microbe can persist in environments with short residence times. In this study, we conducted a chemostat experiment with natural microbial communities and manipulated dilution rate to test how it would act as a selective force controlling community dynamics and microbial diversity. Using both experimental chemostats and trait-based modeling, we examine how the composition of a microbial community collected from a coastal meromictic pond changes as dilution rate increases from 0.1 to 10 d-1. We compare experimental results from 16S rRNA gene amplicon sequences to the output from two different simulations of the trait-based model, one in which maximum specific growth rate is initially evenly distributed across the community and another where maximum specific growth rate traits are pulled from a beta probability distribution that is skewed towards low specific growth rates. Our experimental results match the simulation where the initial natural population is dominated by slow-growing microbes. Our results also highlight the importance of initial trait distributions in modeling community response to environmental changes. ImportanceAll living organisms are constrained by environmental boundaries that govern where growth is possible, such as minimum and maximum temperature or pH. An organisms maximum specific growth rate places a lower bound on the residence or turnover time of a system where an organism can persist without being removed from the system. While we have good bounds on the maximum specific growth rate of culturable organisms, such as Escherichia or Vibrio species, information is lacking on how the maximum specific growth rate trait is distributed in natural microbial communities. This information is critical for understanding how a community will respond to changes in residence time. Using chemostats and trait-based modeling, this study assesses how maximum specific growth rate is distributed in a natural community collected from a coastal, salinity-stratified pond.

microbiology↗

Diel light cycles affect phytoplankton competition in the global ocean

Light, essential for photosynthesis, is present in two periodic cycles in nature: seasonal and diel. Although seasonality of light is typically resolved in ocean ecosystem and biogeochemistry models because of its significance for seasonal succession and biogeography of phytoplankton, the diel light cycle is generally not resolved. Here we use a three-dimensional global ocean model and compare high temporal resolution simulations with and without diel light cycles. The model simulates 15 phytoplankton types of different cell size, encompassing two broad ecological strategies: small cells with high nutrient affinity (gleaners) and larger cells with high maximal growth rate (opportunists). Both are grazed by zooplankton and limited by nitrogen, phosphorus and iron. Simulations show that diel cycles of light induce diel cycles in phytoplankton populations and limiting nutrients in the global ocean. Diel nutrient cycles are associated with higher concentration of limiting nutrients by up to 200% at low latitudes (-40{degrees} to 40{degrees}), a process that increases opportunists biomass by up to 50%. Size classes with the highest maximal growth rates from both gleaner and opportunist groups are favored the most by diel light cycles. This mechanism weakens as latitude increases because the effects of the seasonal cycle dominate over those of the diel cycle. The present work shows that resource competition under diel light cycles has a significant impact on phytoplankton biogeography, indicating the necessity of resolving diel processes in global ocean models.

ecology↗

Seafloor incubation experiment with deep-sea hydrothermal vent fluid reveals effect of pressureand lag time on autotrophic microbial communities

Depressurization and sample processing delays may impact the outcome of shipboard microbial incubations of samples collected from the deep sea. To address this knowledge gap, we developed an ROV-powered incubator instrument to carry out and compare results from in situ and shipboard RNA Stable Isotope Probing (RNA-SIP) experiments to identify the key chemolithoautotrophic microbes and metabolisms in diffuse, low-temperature venting fluids from Axial Seamount. All the incubations showed microbial uptake of labelled bicarbonate primarily by thermophilic autotrophic Epsilonbacteraeota that oxidized hydrogen coupled with nitrate reduction. However, the in situ seafloor incubations showed higher abundances of transcripts annotated for aerobic processes suggesting that oxygen was lost from the hydrothermal fluid samples prior to shipboard analysis. Furthermore, transcripts for thermal stress proteins such as heat shock chaperones and proteases were significantly more abundant in the shipboard incubations suggesting that hydrostatic pressure ameliorated thermal stress in the metabolically active microbes in the seafloor incubations. Together, results indicate that while the autotrophic microbial communities in the shipboard and seafloor experiments behaved similarly, there were distinct differences that provide new insight into the activities of natural microbial assemblages under near-native conditions in the ocean.

microbiology↗

Using maximum entropy production to describe microbial biogeochemistry over time and space in a meromictic pond

The maximum entropy production (MEP) conjecture posits that systems with many degrees of freedom will likely organize to maximize the rate of free energy dissipation. Previous work indicates that biological systems can outcompete abiotic systems by maximizing free energy dissipation over time by utilizing temporal strategies acquired and refined by evolution, and over space via cooperation. In this study, we develop an MEP model to describe biogeochemistry observed in Siders Pond, a phosphate limited meromictic system located in Falmouth, MA that exhibits steep chemical gradients due to density-driven stratification that supports anaerobic photosynthesis as well as microbial communities that catalyze redox cycles involving O, N, S, Fe and Mn. The MEP model uses a metabolic network to represent microbial redox reactions, where biomass allocation and reaction rates are determined by solving an optimization problem that maximizes entropy production over time and a 1D vertical profile constrained by an advection-dispersion-reaction model. We introduce a new approach for modeling phototrophy and explicitly represent aerobic photoautotrophs, anoxygenic photoheterotrophs and anaerobic photoautotrophs. The metabolic network also includes reactions for heterotrophic bacteria, sulfate reducing bacteria, sulfide oxidizing bacteria and aerobic and anaerobic grazers. Model results were compared to observations of biogeochemical constituents collected over a 24 hour period at 8 depths at a single 15 m deep station in Siders Pond. Maximizing entropy production over long (3 d) intervals produced results more similar to field observations than short (0.25 d) interval optimizations, which support the importance of temporal strategies for maximizing entropy production over time. Furthermore, we found that entropy production must be maximized locally instead of globally where energy potentials are degraded quickly by abiotic processes, such as light absorption by water. This combination of field observations with modeling results show that microbial systems in nature can be accurately described by the maximum entropy production conjecture applied over time and space.

systems biology↗