Microbial redox cycling enhances ecosystem thermodynamic efficiency and productivity.

Microbial life in low-energy ecosystems relies on individual energy conservation, optimizing energy use in response to interspecific competition and mutualistic interspecific syntrophy. Our study proposes a novel community-level strategy for increasing energy use efficiency. By utilizing an oxidation-reduction (redox) reaction network model that represents microbial redox metabolic interactions, we investigated multiple species-level competition and cooperation within the network. Our results suggest that microbial functional diversity allows for metabolic handoffs, which in turn leads to increased energy use efficiency. Furthermore, the mutualistic division of labour and the resulting complexity of redox pathways actively drive material cycling, further promoting energy exploitation. Our findings reveal the potential of self-organized ecological interactions to develop efficient energy utilization strategies, with important implications for microbial ecosystem functioning and the co-evolution of life and Earth.

Microbial material cycling, energetic constraints and ecosystem expansion in subsurface ecosystems.

To harvest energy from chemical reactions, microbes engage in diverse catabolic interactions that drive material cycles in the environment. Here, we consider a simple mathematical model for cycling reactions between alternative forms of an element (A and Ae), where reaction 1 converts A to Ae and reaction 2 converts Ae to A. There are two types of microbes: type 1 microbes harness reaction 1, and type 2 microbes harness reaction 2. Each type receives its own catabolic resources from the other type and provides the other type with the by-products as the catabolic resources. Analyses of the model show that each type increases its steady-state abundance in the presence of the other type. The flux of material flow becomes faster in the presence of microbes. By coupling two catabolic reactions, types 1 and 2 can also expand their realized niches through the abundant resource premium, the effect of relative quantities of products and reactants on the available chemical energy, which is especially important for microbes under strong energetic limitations. The plausibility of mutually beneficial interactions is controlled by the available chemical energy (Gibbs energy) of the system. We conclude that mutualistic catabolic interactions can be an important factor that enables microbes in subsurface ecosystems to increase ecosystem productivity and expand the ecosystem.

The fitness of chemotrophs increases when their catabolic by-products are consumed by other species.

Chemotrophic microorganisms synthesise biomass by utilising energy obtained from a set of chemical reactions that convert resources to by-products, forming catabolic interactions. The amount of energy obtained per catabolic reaction decreases with the abundance of the by-product named as the 'abundant resource premium'. Consider two species, Species 1 and 2, Species 1 obtains energy from a reaction that converts resource A to by-product B. Species 2 then utilises B as its resource, extracting energy from a reaction that converts B to C. Thus, the presence of Species 2 reduces the abundance of B, which improves the fitness of Species 1 by increasing the energy acquisition per reaction of A to B. We discuss the population dynamic implication of this effect and its importance in expanding a realised niche, boosting material flow through the ecosystem and providing mutualistic interactions among species linked by the material flow. Introducing thermodynamics into population ecology could offer us fundamental ecological insights into understanding the ecology of chemotrophic microorganisms dominating the subsurface realm.

Potential for Aerobic Methanotrophic Metabolism on Mars.

Observational evidence supports the presence of methane (CH4) in the martian atmosphere on the order of parts per billion by volume (ppbv). Here, we assess whether aerobic methanotrophy is a potentially viable metabolism in the martian upper regolith, by calculating metabolic energy gain rates under assumed conditions of martian surface temperature, pressure, and atmospheric composition. Using kinetic parameters for 19 terrestrial aerobic methanotrophic strains, we show that even under the imposed low temperature and pressure extremes (180-280 K and 6-11 hPa), methane oxidation by oxygen (O2) should in principle be able to generate the minimum energy production rate required to support endogenous metabolism (i.e., cellular maintenance). Our results further indicate that the corresponding metabolic activity would be extremely low, with cell doubling times in excess of 4000 Earth years at the present-day ppbv-level CH4 mixing ratios in the atmosphere of Mars. Thus, while aerobic methanotrophic microorganisms similar to those found on Earth could theoretically maintain their vital functions, they are unlikely to constitute prolific members of hypothetical martian soil communities.

Population dynamics of chemotrophs in anaerobic conditions where the metabolic energy acquisition per redox reaction is limited.

We present a new model of microbial population growth that focuses on the acquisition of metabolic energy through chemosynthesis and how this depends on the concentration of resources and byproducts. Due to entropy effects, organisms extract the greater energy (i.e., they produce the greater amount of adenosine triphosphate) when they use resources that are abundant and generates byproducts that are rare. This effect, which we call the "abundant resource premium," has been neglected in traditional models of microbial growth because the total metabolic energy acquisition is generally far greater than this premium. This term, however, cannot be neglected for many microbes, such as sulfate reducers, iron oxidizers, and methanogens, which live under conditions of low-energy availability. Our model showed qualitatively different behaviors from those observed in traditional microbial population growth models, such as the Monod model. For example, the steady-state population density was maximum at an intermediate resource-utilizing ability, suggesting that high substrate acquisition is not always advantageous for a microbial population when the availability of metabolic energy is low. We discuss possible implications for evolutionary and ecosystem sciences.

Assessment of Instructions on Protection Against Food Contaminated with Radiocesium in Japan in 2011.

The Japan Ministry of Health, Labour and Welfare (MHLW) has published instructions for radiological protection against food after the Fukushima Daiichi nuclear power plant accident in 2011. Following the instructions, the export and consumption of food items identified as being contaminated were restricted for a certain period. We assessed the validity of the imposed restriction periods for two representative vegetables (spinach and cabbage) grown in Fukushima Prefecture from two perspectives: effectiveness for reducing dietary dose and economic efficiency. To assess effectiveness, we estimated the restriction period required to maintain consumers' dose below the guidance dose levels. To assess economic efficiency, we estimated the restriction period that maximizes the net benefit to taxpayers. All estimated restriction periods were shorter than the actual restriction periods imposed on spinach and cabbage from Fukushima in 2011, which indicates that the food restriction effectively maintained consumers' dietary dose below the guidance dose level, but in an economically inefficient manner. We also evaluated the response of the restriction period to the sample size for each weekly food safety test and the instructions for when to remove the restriction. Stringent MHLW instructions seemed to sufficiently reduce consumers' health risk even when the sample size for the weekly food safety test was small, but tended to increase the economic cost to taxpayers.

Sample size allocation for food item radiation monitoring and safety inspection.

The objective of this study is to identify a procedure for determining sample size allocation for food radiation inspections of more than one food item to minimize the potential risk to consumers of internal radiation exposure. We consider a simplified case of food radiation monitoring and safety inspection in which a risk manager is required to monitor two food items, milk and spinach, in a contaminated area. Three protocols for food radiation monitoring with different sample size allocations were assessed by simulating random sampling and inspections of milk and spinach in a conceptual monitoring site. Distributions of (131)I and radiocesium concentrations were determined in reference to (131)I and radiocesium concentrations detected in Fukushima prefecture, Japan, for March and April 2011. The results of the simulations suggested that a protocol that allocates sample size to milk and spinach based on the estimation of (131)I and radiocesium concentrations using the apparent decay rate constants sequentially calculated from past monitoring data can most effectively minimize the potential risks of internal radiation exposure.

The effect of zinc on aquatic microbial ecosystems and the degradation of dissolved organic matter.

We developed a simple aquatic microbial ecosystem model in order to examine potential effects of zinc on microorganisms and the related degradation of dissolved organic matter (DOM). The model is a combination of both a traditional food chain and a microbial loop. The traditional food chain is mainly composed of phytoplankton and zooplankton, whilst the microbial loop is composed of DOM, bacteria and bacterivorous protozoa. We incorporated the suppressive effect of zinc on the bacterial uptake of DOM and assessed the steady state responses of the model for various zinc concentrations. The analytical and numerical results of the model implied that either zooplankton or bacterivorous protozoa might be the most vulnerable group to excessive zinc load than bacteria, depending on the grazing preference of zooplankton between phytoplankton and bacterivorous protozoa. The sensitivity analyses supported that the microbial loop solely is more sensitive to zinc than the coupled system combining both the traditional food chain and the microbial loop.

Individual and combined suppressive effects of submerged and floating-leaved macrophytes on algal blooms.

Shallow lakes and ponds are often characterised either by clear water with abundant submerged macrophytes or by turbid water with abundant phytoplankton. Blooms of toxic filamentous blue-green algae (cyanobacteria) often dominate the phytoplankton community in eutrophic lakes, which threatens ecological functions and biodiversity of freshwater ecosystems. We studied a simple lake model in order to evaluate individual and combined suppressive effects of rooted submerged and rooted floating-leaved macrophytes on algal blooms. Floating-leaved plants are superior competitors for light, whereas submerged plants absorb and reduce available phosphorus in a water column that rooted floating-leaved plants exploit to a lesser extent. We found that mixed vegetation that includes both submerged and floating-leaved plants is more resistant than vegetation comprised by a single plant type to algal invasion triggered by phosphorus loading. In addition, competitive exclusion of submerged plants by floating-leaved plants may promote an algal bloom. These predictions were confirmed by the decision tree analysis of field data from 35 irrigation ponds in Hyogo Prefecture, Japan.

Regime shift and robustness of organism-created environments: A model for microbial ecosystems.

Organism-environment interactions are different from organism-resource interactions in two respects: (1) resources can only be consumed by organisms whereas environmental conditions can be increased or decreased depending on the species; (2) high resource conditions generally stimulate the growth of organisms, whereas extreme environmental conditions are not necessarily favored because each species usually has an optimum range for growth. To investigate the properties of an organism-environment feedback system, we analyze a model for microbial ecosystems in which a single microorganism species can modify the environmental pH. We demonstrate that the equilibrium level of the environmental pH can be partially regulated at a relatively constant value even if the pH in the influx to the ecosystem changes over a wide range. For species that acidify the medium, the equilibrium pH is somewhat lower than the pH optimal for the species. The pH-stabilizing effect of microorganisms is stronger if their growth is self-limited by the environmental pH. When the influx becomes sufficiently alkaline, the population of the organism suddenly disappears and the environmental pH changes abruptly. The system shows bi-stability and hysteresis and therefore differs from a standard resource competition model composed of a single species that consumes resources.

Mathematical explanation for the non-linear hydrophobicity-dependent bioconcentration processes of persistent organic pollutants in phytoplankton.

Phytoplankton play a vital role in determining the fate and transport of persistent organic pollutants (POPs) in aquatic ecosystems. Lipids in phytoplankton cells can accumulate POPs, and equilibrium partitioning of the chemicals between lipids and water can be deduced from the octanol/water partition coefficient (K(ow)). However, there is much uncertainty in the response of the bioconcentration factor (BCF) to K(ow). While distinct level-off and bell-shaped responses of BCF to K(ow) have been confirmed by laboratory experiments, a mathematical basis for the non-linear processes has been lacking. Using two differential equation models (Water-Phytoplankton and Water-Phytoplankton-Dissolved Organic Carbon) we here examine previously reported non-linearity between BCF and K(ow). Our modelling studies suggest that a level-off response of the true BCF (BCF estimated at equilibrium) to K(ow) could be attributed to the presence of dissolved organic carbon (DOC). The alternative bell-shaped response appears to be a consequence of the apparent BCF (BCF estimated at non-equilibrium) for which the slow uptake rate of chemical compounds of relatively large molecular mass by phytoplankton is responsible.

Coexistence introducing regulation of environmental conditions.

Interactions between environmental conditions and environment-affecting species have not been investigated extensively. In this study, the population dynamics of species yielding regulative feedback between temperature (a representative of environmental condition) and species with a temperature-altering trait was examined. We considered a simple closed model that described the population of two species (at least one of them had a temperature-altering trait) competing for one resource. The long-term outcomes of the competition and changes of temperature were explored against increasing background temperature. As a result of simulations, the regulation of temperature was accompanied by the coexistence of two species, which was contrary to the 'Gause's exclusion principle'. The steady-state analysis showed that (i) the temperature-altering trait allowed species to coexist and (ii) the coexistence of species with the trait could introduce the regulation of temperature. A 'trade-off' in their ability to utilize a resource plays a key role in this coexistence and homeostasis of temperature. This may imply that actual environmental conditions can be automatically stabilized by resource competition among species in natural ecosystems.

Nitric oxide decreases cell surface expression of aquaporin-5 and membrane water permeability in lung epithelial cells.

Nitric oxide (NO) is implicated in the pathogenesis of lung inflammation and edema. In this study, the effects of nitric oxide (NO)-donors on membrane water permeability and cell surface expression of aquaporin-5 (AQP5) in mouse lung epithelial cells were examined. NO-donors, GSNO and NOC-18 decreased cell surface expression of AQP5, concentration- and time-dependently, whereas they did not affect the amount of AQP5 in whole cell lysates. The membrane water permeability of cells was also decreased by treatment with NO-donors. The decrease in cell surface AQP5 by NO was abolished by simultaneous treatment with methyl-beta-cyclodextrin, but not with ODQ, an inhibitor of the cGMP-dependent pathway. In addition, immunocytochemistry with anti-AQP5 indicated that NO changed AQP5 localization from the plasma membrane to the intracellular fraction. These data indicate that NO stimulates AQP5 internalization from the plasma membrane through a cGMP-independent mechanism, and decreases membrane water permeability.

All-trans retinoic acid increases expression of aquaporin-5 and plasma membrane water permeability via transactivation of Sp1 in mouse lung epithelial cells.

Aquaporin-5 (AQP5) is a water-selective channel protein that is expressed in lacrimal glands, salivary glands, and distal lung. Several studies using AQP5 knockout mice have revealed that AQP5 plays an important role in maintaining water homeostasis in the lung. We report here that all-trans retinoic acid (atRA) increases plasma membrane water permeability, AQP5 mRNA and protein expression, and AQP5 promoter activity in MLE-12 cells. The promoter activation induced by atRA was diminished by mutation at the Sp1/Sp3 binding element (SBE), suggesting that the SBE mediates the effects of atRA. In addition, atRA increased the binding of Sp1 to the SBE without changing the levels of Sp1 in the nucleus. Taken together, our data indicate that atRA increases AQP5 expression through transactivation of Sp1, leading to an increase in plasma membrane water permeability.

Daisyworld inhabited with daisies incorporating a seed size/number trade-off: the mechanism of negative feedback on selection from a standpoint of the competition theory.

We reexamined a Daisyworld model from the traditional view of competition theory. Unlike the original model, white and black daisies in our model incorporate a seeding/germination trade-off against bare ground area without assuming the local temperature reward. As a result, the planetary temperature is automatically regulated by two species if the following conditions are met: (i) the species react equally to an environmental condition, but one can alter the environmental condition in the opposite direction to the other. (ii) that one of the two cannot have both a higher maximal growth rate (mu(max)) and lower half-saturation constant (K) than those of the other. In other words, a pair of phenotypes incorporates a trade-off between quality and number of seeds. We found that the homeostatic regulation can also be reconciled with the adaptive evolution of optimal temperature. The results of simulation imply that biotic environmental feedback can also be maintained when the emergence of polymorphisms (black and white daisies) is closely linked to such a trade-off.