Microorganisms buried in marine sediments are known to endure starvation over geologic timescales. However, the mechanisms of how these microorganisms cope with prolonged energy limitation is unknown and therefore yet to be captured in a quantitative framework. Here, we present a novel mathematical model that considers (a) the physiological transitions between the active and dormant states of microorganisms, (b) the varying requirement for maintenance power between these phases, and (c) flexibility in the provenance (i.e., source) of energy from exogenous and endogenous catabolism. The model is applied to sediments underlying the oligotrophic South Pacific Gyre where microorganisms endure ultra‐low fluxes of energy for tens of millions of years. Good fits between model simulations and measurements of cellular carbon and organic carbon concentrations are obtained and are interpreted as follows: (a) the unfavourable microbial habitat in South Pacific Gyre sediments triggers rapid mortality and a transition to dormancy; (b) there is minimal biomass growth, and organic carbon consumption is dominated by catabolism to support maintenance activities rather than new biomass synthesis; (c) the amount of organic carbon that microorganisms consume for maintenance activities is equivalent to approximately 2% of their carbon biomass per year; and (d) microorganisms must rely solely on exogenous rather than endogenous catabolism to persist in South Pacific Gyre sediments over long timescales. This leads us to the conclusion that under oligotrophic conditions, the fitness of an organism is determined by its ability to simply stay alive, rather than to grow. This modelling framework is designed to be flexible for application to other sites and habitats, and thus serves as a new quantitative tool for determining the habitability of and an ultimate limit for life in any environment.
The in situ production of necromass and its role as a power source in sustaining heterotrophic microorganisms in natural settings has never been quantified. Here, we quantify the power availability from necromass oxidation to living microorganisms buried in marine sediments over millions of years, first in the oligotrophic South Pacific Gyre (SPG), and second on a global scale. We calculate that power from autochthonously produced necromass in the upper meter of sediment at SPG provides only a small fraction (~0.02%) of the maintenance power demand of the living community (1.9×10-19 W cell-1). Power from necromass oxidation diminishes considerably with increasing sediment depth (and thus sediment age). Alternatively, the oxidation of allochthonous organic matter, and of radiolytic H2, provides power equivalent to or in excess of the maintenance demands of living microorganisms at SPG. On a global scale, necromass may support the maintenance power demand of 2 to 13% of the microbial community in relatively young sediments (<10,000 years) when it is oxidized with SO42- and O2 respectively. However, in older sediments, the power supplied by necromass is negligible (<0.01%). Nevertheless, the oxidation of a single dead cell per year provides sufficient power to support the maintenance demands of dozens to thousands of cells in low-energy marine sediments. This raises the possibility that the production and oxidation of necromass may provide a mechanism for non-growing microorganisms to endure unfavorable, low-energy settings over geological timescales.
Marine sediments constitute one of the most energy-limited habitats on Earth, in which microorganisms persist over extraordinarily long timescales with very slow metabolisms. This habitat provides an ideal environment in which to study the energetic limits of life. However, the bioenergetic factors that can determine whether microorganisms will grow, lie dormant, or die, as well as the selective environmental pressures that determine energetic trade-offs between growth and maintenance activities, are not well understood. Numerical models will be pivotal in addressing these knowledge gaps. However, models rarely account for the variable physiological states of microorganisms and their demand for energy. Here, we review established modeling constructs for microbial growth rate, yield, maintenance, and physiological state, and then provide a new model that incorporates all of these factors. We discuss this new model in context with its future application to the marine subsurface. Understanding the factors that regulate cell death, physiological state changes, and the provenance of maintenance energy (i.e., endogenous versus exogenous metabolism), is crucial to the design of this model. Further, measurements of growth rate, growth yield, and basal metabolic activity will enable bioenergetic parameters to be better constrained. Last, biomass and biogeochemical rate measurements will enable model simulations to be validated. The insight provided from the development and application of new microbial modeling tools for marine sediments will undoubtedly advance the understanding of the minimum power required to support life, and the ecophysiological strategies that organisms utilize to cope under extreme energy limitation for extended periods of time.
Ancient putative microbial structures that appear in the rock record commonly serve as evidence of early life on Earth, but the details of their formation remain unclear. The study of modern microbial mat structures can help inform the properties of their ancient counterparts, but modern mineralizing mat systems with morphological similarity to ancient structures are rare. Here, we characterize partially lithified microbial mats containing cm-scale dendrolitic coniform structures from a geothermal pool (“Cone Pool”) at Little Hot Creek, California, that if fully lithified, would resemble ancient dendrolitic structures known from the rock record. Light and electron microscopy revealed that the cm-scale ‘dendrolitic cones’ were comprised of intertwined microbial filaments and grains of calcium carbonate. The degree of mineralization (carbonate content) increased with depth in the dendrolitic cones. Sequencing of 16S rRNA gene libraries revealed that the dendrolitic cone tips were enriched in OTUs most closely related to the genera Phormidium, Leptolyngbya, and Leptospira, whereas mats at the base and adjacent to the dendrolitic cones were enriched in Synechococcus. We hypothesize that the consumption of nutrients during autotrophic and heterotrophic growth may promote movement of microbes along diffusive nutrient gradients, and thus microbialite growth. Hour-glass shaped filamentous structures present in the dendrolitic cones may have formed around photosynthetically-produced oxygen bubbles—suggesting that mineralization occurs rapidly and on timescales of the lifetime of a bubble. The dendrolitic-conical structures in Cone Pool constitute a modern analog of incipient microbialite formation by filamentous microbiota that are morphologically distinct from any structure described previously. Thus, we provide a new model system to address how microbial mats may be preserved over geological timescales.
The recent retreat of glaciers and ice sheets as a result of global warming exposes forefield soils that are rapidly colonized by microbes. These ecosystems are dominant in high-latitude carbon and nutrient cycles as microbial activity drives biogeochemical transformations within these newly exposed soils. Despite this, little is known about the response of these emerging ecosystems and associated biogeochemical cycles to projected changes in environmental factors due to human impacts. Here, we applied the model SHIMMER to quantitatively explore the sensitivity of biogeochemical dynamics in the forefield of Midtre Lovénbreen, Svalbard, to future changes in climate and anthropogenic forcings including soil temperature, snow cover, and nutrient and organic substrate deposition. Model results indicated that the rapid warming of the Arctic, as well as an increased deposition of organic carbon and nutrients, may impact primary microbial colonizers in Arctic soils. Warming and increased snow-free conditions resulted in enhanced bacterial production and an accumulation of biomass that was sustained throughout 200 years of soil development. Nitrogen deposition stimulated growth during the first 50 years of soil development following exposure. Increased deposition of organic carbon sustained higher rates of bacterial production and heterotrophic respiration leading to decreases in net ecosystem production and thus net CO2 efflux from soils. Pioneer microbial communities were particularly susceptible to future changes. All future climate simulations encouraged a switch from allochthonously-dominated young soils (<40 years) to microbially-dominated older soils, due to enhanced heterotrophic degradation of organic matter. Critically, this drove remineralisation and increased nutrient availability. Overall, we show that human activity, especially the burning of fossil fuels and the enhanced deposition of nitrogen and organic carbon, has the potential to considerably affect the biogeochemical development of recently exposed Arctic soils in the present day and for centuries into the future. These effects must be acknowledged when attempting to make accurate predictions of the future fate of Arctic soils that are exposed over large expanses of presently ice-covered regions.
Microorganisms buried in marine sediments endure prolonged energy-limitation over geological timescales. My research within C-DEBI is motivated by the quest to determine and understand activity levels among microbial communities in the marine subsurface in relation to their geochemical and physical environment. To this end, in collaboration with Doug LaRowe and Jan Amend (USC), I developed novel modelling frameworks based on thermodynamic and microbial-modelling principles to explore and quantify:
The energy sources to deeply buried microorganisms and their demand for energy.
The activity of microorganisms and the factors that determine physiological transitions between active and dormant states.
The varying energy requirements of active and dormant microbes and the allocation of energy between maintenance and growth.
The cell-specific energy utilization (i.e. power) of subsurface life on a global scale.
I led the development of a new freely-available and open-source platform MicroLow 1.0 – a process-based microbial model that explicitly considers physiological state transitions and energy for maintenance and growth. Using this model, I showed that energetic efficiency provides a selective advantage for long-term microbial survival in oligotrophic marine sediments.
Numerous additional opportunities have arisen thanks to the C-DEBI program and community, including participation in two collaborative workshops (organic carbon preservation, impacts of deep sea mining), numerous valuable interactions, ongoing collaborations and spin-off projects, presentations at international conferences, professional development opportunities, media exposure, complementary funding including a Deep Carbon Observatory DLMV Fellowship, significant widening of my professional network, fieldwork opportunities, and career progression.