James A. Bradley

Microbial community dynamics in the forefield of glaciers

Retreating ice fronts (as a result of a warming climate) expose large expanses of deglaciated forefield, which become colonized by microbes and plants. There has been increasing interest in characterizing the biogeochemical development of these ecosystems using a chronosequence approach. Prior to the establishment of plants, microbes use autochthonously produced and allochthonously delivered nutrients for growth. The microbial community composition is largely made up of heterotrophic microbes (both bacteria and fungi), autotrophic microbes and nitrogen-fixing diazotrophs. Microbial activity is thought to be responsible for the initial build-up of labile nutrient pools, facilitating the growth of higher order plant life in developed soils. However, it is unclear to what extent these ecosystems rely on external sources of nutrients such as ancient carbon pools and periodic nitrogen deposition. Furthermore, the seasonal variation of chronosequence dynamics and the effect of winter are largely unexplored. Modelling this ecosystem will provide a quantitative evaluation of the key processes and could guide the focus of future research. Year-round datasets combined with novel metagenomic techniques will help answer some of the pressing questions in this relatively new but rapidly expanding field, which is of growing interest in the context of future large-scale ice retreat.

Aerobiology over Antarctica – a new initiative for atmospheric ecology

The role of aerial dispersal in shaping patterns of biodiversity remains poorly understood, mainly due to a lack of coordinated efforts in gathering data at appropriate temporal and spatial scales. It has been long known that the rate of dispersal to an ecosystem can significantly influence ecosystem dynamics, and that aerial transport has been identified as an important source of biological input to remote locations. With the considerable effort devoted in recent decades to understanding atmospheric circulation in the south-polar region, a unique opportunity has emerged to investigate the atmospheric ecology of Antarctica, from regional to continental scales. This concept note identifies key questions in Antarctic microbial biogeography and the need for standardized sampling and analysis protocols to address such questions. A consortium of polar aerobiologists is established to bring together researchers with a common interest in the airborne dispersion of microbes and other propagules in the Antarctic, with opportunities for comparative studies in the Arctic.

Bridging the divide: a model-data approach to Polar and Alpine microbiology.

Advances in microbial ecology in the cryosphere continue to be driven by empirical approaches including field sampling and laboratory-based analyses. Although mathematical models are commonly used to investigate the physical dynamics of Polar and Alpine regions, they are rarely applied in microbial studies. Yet integrating modelling approaches with ongoing observational and laboratory-based work is ideally suited to Polar and Alpine microbial ecosystems given their harsh environmental and biogeochemical characteristics, simple trophic structures, distinct seasonality, often difficult accessibility, geographical expansiveness and susceptibility to accelerated climate changes. In this opinion paper, we explain how mathematical modelling ideally complements field and laboratory-based analyses. We thus argue that mathematical modelling is a powerful tool for the investigation of these extreme environments and that fully integrated, interdisciplinary model-data approaches could help the Polar and Alpine microbiology community address some of the great research challenges of the 21st century (e.g. assessing global significance and response to climate change). However, a better integration of field and laboratory work with model design and calibration/validation, as well as a stronger focus on quantitative information is required to advance models that can be used to make predictions and upscale processes and fluxes beyond what can be captured by observations alone.

Carbonate-rich dendrolitic cones: insights into a modern analog for incipient microbialite formation, Little Hot Creek, Long Valley Caldera, California

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.Paleobiology: modern microbes may tell an ancient taleMicrobial mats currently thriving in a hot pool in California may help explain the origin of fossilized evidence of early life on Earth. Modern microbial mats that are structurally similar to microbial fossil mats are rare. John Spear at the Colorado School of Mines, with co-workers from elsewhere in the USA and in Chile, examined the microbial mats growing in a geothermal pool at Little Hot Creek in California. Light microscopy and electron microscopy identified crucial fine structure similarities with branching mat structures in the fossil record. The researchers developed hypotheses to explain the influence of nutrient flow on the growth and movement of the microbes in the mats. These living mats are a useful model system to help researchers understand how ancient microbial mats formed and were preserved over geological timescales.

Bioenergetic Controls on Microbial Ecophysiology in Marine Sediments

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.

Ecological Modeling of the Supraglacial Ecosystem: A Process-based Perspective

Glacier and ice sheet surfaces are important microbe-dominated ecosystems that are changing rapidly due to climate change, with potentially significant impacts. A theoretical framework of the supraglacial (glacier surface) ecosystem is needed to enable its mathematical modelling, a necessary tool for understanding, quantifying and predicting present day and future ecosystem dynamics. Here we review key biological processes occurring on glacier and ice sheet surfaces and present three frameworks for constructing process-based models of the surface ecosystem, using the largest supraglacial ecosystem on Earth – the Greenland ice sheet surface – as an important example. The models are based on organic carbon transformations, but vary in numerical complexity and in the level of detail of biological processes. This perspective is intended to guide future supraglacial ecosystem model development, field data collection for parameterisation and validation purposes, and encourage inter-disciplinary collaboration between modellers and experimentalists.

Survival of the fewest: Microbial dormancy and maintenance in marine sediments through deep time

Abstract 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.

Microbial and biogeochemical dynamics in glacier forefields are sensitive to century-scale climate and anthropogenic change

The recent retreat of glaciers and ice sheets as a result of global warming exposes forefield soils that are rapidly colonised 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 Lovenbreen, 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 colonisers 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.