Microorganisms and their roles in fundamental biogeochemical cycles

Biogeochemistry is the discipline that strives to understand intricate processes, often microbially mediated ones, that transform and recycle both organic and inorganic substances in soils, sediments, and waters. These processes, manifestations of diverse and highly evolved cellular mechanisms catalyzed by Bacteria and Archaea, maintain the biosphere. Progress in biogeochemistry relies upon the underlying science of environmental microbiology. Over the last 2 years, important discoveries have advanced the ecological, physiological, biochemical, and genomic bases for a variety of microbiological processes including anaerobic methane oxidation, photosynthesis, phosphorous uptake, biodegradation of organic pollutants, and numerous aspects of the nitrogen and sulfur cycles. Here recent literature is assessed and placed within a five-stage paradigm for making scientific progress in environmental microbiology, biogeochemistry, and biotechnology.     

The role of phytoplankton photosynthesis in global biogeochemical cycles

Phytoplankton biomass in the world's oceans amounts to only 1–2% of the total global plant carbon, yet these organisms fix between 30 and 50 billion metric tons of carbon annually, which is about 40% of the total. On geological time scales there is profound evidence of the importance of phytoplankton photosynthesis in biogeochemical cycles. It is generally assumed that present phytoplankton productivity is in a quasi steady-state (on the time scale of decades). However, in a global context, the stability of oceanic photosynthetic processes is dependent on the physical circulation of the upper ocean and is therefore strongly influenced by the atmosphere. The net flux of atmospheric radiation is critical to determining the depth of the upper mixed layer and the vertical fluxes of nutrients. These latter two parameters are keys to determining the intensity, and spatial and temporal distributions of phytoplankton blooms. Atmospheric radiation budgets are not in steady-state. Driven largely by anthropogenic activities in the 20th century, increased levels of IR- absorbing gases such as CO₂, CH₄ and CFC's and NO_x will potentially increase atmospheric temperatures on a global scale. The atmospheric radiation budget can affect phytoplankton photosynthesis directly and indirectly. Increased temperature differences between the continents and oceans have been implicated in higher wind stresses at the ocean margins. Increased wind speeds can lead to higher nutrient fluxes. Throughout most of the central oceans, nitrate concentrations are sub-micromolar and there is strong evidence that the quantum efficiency of Photosystem II is impaired by nutrient stress. Higher nutrient fluxes would lead to both an increase in phytoplankton biomass and higher biomass-specific rates of carbon fixation. However, in the center of the ocean gyres, increased radiative heating could reduce the vertical flux of nutrients to the euphotic zone, and hence lead to a reduction in phytoplankton carbon fixation. Increased desertification in terrestrial ecosystems can lead to increased aeolean loadings of essential micronutrients, such as iron. An increased flux of aeolean micronutrients could fertilize nutrient-replete areas of the open ocean with limiting trace elements, thereby stimulating photosynthetic rates. The factors which limit phytoplankton biomass and photosynthesis are discussed and examined with regard to potential changes in the Earth climate system which can lead the oceans away from steady-state. While it is difficult to confidently deduce changes in either phytoplankton biomass or photosynthetic rates on decadal time scales, time-series analysis of ocean transparency data suggest long-term trends have occurred in the North Pacific Ocean in the 20th century. However, calculations of net carbon uptake by the oceans resulting from phytoplankton photosynthesis suggest that without a supply of nutrients external to the ocean, carbon fixation in the open ocean is not presently a significant sink for excess atmospheric CO₂.The submitted paper has been authored under Contract No. DE-AC02-76H00016 with the US Department of Energy. Accordingly, the US Government retains a non-exclusive, royalty-free license to publish or reproduce the published form of this contribution, or allow others to do so, for US Government purposes.     

Transpiration and canopy conductance in a pristine broad-leaved forest of Nothofagus: an analysis of xylem sap flow and eddy correlation measurements

Summary Tree transpiration was determined by xylem sap flow and eddy correlation measurements in a temperate broad-leaved forest of Nothofagus in New Zealand (tree height: up to 36 m, one-sided leaf area index: 7). Measurements were carried out on a plot which had similar stem circumference and basal area per ground area as the stand. Plot sap flux density agreed with tree canopy transpiration rate determined by the difference between above-canopy eddy correlation and forest floor lysimeter evaporation measurements. Daily sap flux varied by an order of magnitude among trees (2 to 87 kg day^–1 tree^–1). Over 50% of plot sap flux density originated from 3 of 14 trees which emerged 2 to 5 m above the canopy. Maximum tree transpiration rate was significantly correlated with tree height, stem sapwood area, and stem circumference. Use of water stored in the trees was minimal. It is estimated that during growth and crown development, Nothofagus allocates about 0.06 m of circumference of main tree trunk or 0.01 m² of sapwood per kg of water transpired over one hour.Maximum total conductance for water vapour transfer (including canopy and aerodynamic conductance) of emergent trees, calculated from sap flux density and humidity measurements, was 9.5 mm s^–1 that is equivalent to 112 mmol m^–2 s^–1 at the scale of the leaf. Artificially illuminated shoots measured in the stand with gas exchange chambers had maximum stomatal conductances of 280 mmol m^–2 s^–1 at the top and 150 mmol m^–2 s^–1 at the bottom of the canopy. The difference between canopy and leaf-level measurements is discussed with respect to effects of transpiration on humidity within the canopy. Maximum total conductance was significantly correlated with leaf nitrogen content. Mean carbon isotope ratio was –27.76±0.27 (average ±s.e.) indicating a moist environment. The effects of interactions between the canopy and the atmosphere on forest water use dynamics are shown by a fourfold variation in coupling of the tree canopy air saturation deficit to that of the overhead atmosphere on a typical fine day due to changes in stomatal conductance.This paper is dedicated to Prof. Dr. O.L. Lange on the occasion of his 65th birthday     

Plant protein inhibitors of enzymes: their role in animal nutrition and plant defence

A series of review articles by authors of the Institute of Biology's ‘Studies in Biology’ series (published by Edward Arnold) intended to keep teachers up to date on current ideas in particular areas of biology     

The role of woody detritus in biogeochemical cycles: past,present, and future

Biogeochemistry - Woody detritus (WD), created by mortality of trees and their associated parts, is an important component of forested ecosystems with roles in energy flow, hydrologic and...     

Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition

Plants release a multitude of organic compounds into the rhizosphere, some of which are flavonoids. These products of secondary metabolism are mainly studied for their antioxidant properties and for their role in the establishment of rhizobium-legume symbiosis; however, it has been recently demonstrated that flavonoids can also affect nutrient availability through soil chemical changes. This review will give an overview of the types and amounts of flavonoids released by roots of different plant species, as well as summarize the available knowledge on root exudation mechanisms. Subsequently, factors influencing their release will be reported, and the methodological approaches used in the literature will be critically described. Finally, the direct contribution of plant-borne flavonoids on the nitrogen, phosphorous and iron availability into the rhizosphere will be discussed.     

Arbuscular mycorrhizas and their role in plant growth, nitrogen interception and soil gas efflux in an organic production system

Background and aims

Roots and mycorrhizas play an important role in not only plant nutrient acquisition, but also ecosystem nutrient cycling.

Methods

A field experiment was undertaken in which the role of arbuscular mycorrhizas (AM) in the growth and nutrient acquisition of tomato plants was investigated. A mycorrhiza defective mutant of tomato (Solanum lycopersicum L.) (named rmc) and its mycorrhizal wild type progenitor (named 76R) were used to control for the formation of AM. The role of roots and AM in soil N cycling was studied by injecting a ¹⁵N-labelled nitrate solution into surface soil at different distances from the 76R and rmc genotypes of tomato, or in plant free soil. The impacts of mycorrhizal and non-mycorrhizal root systems on soil greenhouse gas (CO₂ and ¹⁴⁺¹⁵N₂O and ¹⁵N₂O) emissions, relative to root free soils, were also studied.

Results

The formation of AM significantly enhanced plant growth and nutrient acquisition, including interception of recently applied NO ₃ ^? . Whereas roots caused a small but significant decrease in ¹⁵N₂O emissions from soils at 23?h after labeling, compared to the root-free treatment, arbuscular mycorrhizal fungi (AMF) had little effect on N₂O emissions. In contrast soil CO₂ emissions were higher in plots containing mycorrhizal root systems, where root biomass was also greater.

Conclusions

Taken together, these data indicate that roots and AMF have an important role to play in plant nutrient acquisition and ecosystem N cycling.     

The effect of deficit irrigation on seasonal variations of plant water use in Olea europaea L.

A field experiment on olive trees (Olea europaea L.) was designed with the objective to search for an optimum irrigation scheduling by analyzing the possible effects of deficit irrigation. Treatments were: a non-irrigated control (rainfed) and three treatments that received seasonal water amount equivalent to 33 and 66% of crop evapotranspiration (ET_C) in the period August–September (respectively 33II and 66II), and 66% of (ET_C) from late May to early October (66I-II). Atmospheric evaporative demand and soil moisture conditions were regularly monitored. Irrigation effects on plant water relations were characterized throughout a growing season. Whole-plant water use, in deficit irrigated (66I-II) and rainfed olive trees, was determined using a xylem sap flow method (compensation heat-pulse technique). The magnitude of variations in water use and the seasonal dynamic of water relations varied among treatments, suggesting that olive trees were strongly responsive to both irrigation amount and time. Physiological parameters responded to variations in tree water status, soil moisture conditions and atmospheric evaporative demand. All measurements of tree water status were highly correlated with one another. There was a considerable degree of agreement between daily transpiration deduced from heat-pulse velocity and that determined by calibration using the water balance technique. Deficit irrigation during the whole summer (66I-II) resulted in improved plant water relations with respect to other watering regimes; while, severe regulated deficit irrigation differentiated only slightly 33II treatment from rainfed plants. Nevertheless, regulated deficit irrigation of olive trees after pit hardening (66II) could be recommended, at least in soil, cultivar and environmental conditions of this study.     

Gas exchange in leaves of the root hemiparasitemelampyrum arvense L. before and after attachment to the host plant

Gas exchange characteristics of a hemiparasiteMelampyrum arvense L. before and after attachment to the hostCapsella bursa pastoris (L.) Med. were compared. The net photosynthetic rates (P_N) on a leaf area basis were extremely low and in comparison to the value obtained for the host were about 15 % and 23 % for the unattached and attached hemiparasite, respectively. Also the concentration of photosynthetic pigments was low (as compared with the host the content of chlorophylls was about 33 % and 49 % and of carotenoids about 38 % and 36 % in the unattached and attached hemiparasite, respectively). On the other hand the rates of respiration were high (about 1.8 and 2.6 times higher in the unattached and attached hemiparasite, respectively, than in the host). In darkness stomatal conductance (g_S) of the host and the unattached hemiparasite was rapidly reduced to 10 % of the value obtained in light, g_S of the attached hemiparasite was decreased only by about 30%. A total reduction of g_S occurred at relative water content (RWC) of 85 %, 75% and 45 % for the unattached hemiparasite, the host, and the attached hemiparasite, respectively. The transpiration (E) rate in the preparasitic stage was very low, being 2.6 and 4.5 times smaller than in the host and the attached hemiparasite, respectively. In the attached hemiparasite WUE was 7.5 and 3 times poorer than in the host and in the preparasitic stage, respectively.     

The role of ion channels in plant nutrition and prospects for their genetic manipulation

Ion channels can function in three physiological modes through their ability to: 1) accommodate osmotically significant fluxes over short periods; 2) propagate signals along or across membranes; 3) control the membrane potential. With respect to mineral nutrition it is via the control of the membrane potential that ion channels are probably most significant. In this paper the physiology and prospects for molecular biology of plant ion channels are discussed. It is concluded that identifying and altering the primary structures that determine functional characteristics of plant ion channel genes could result in changes in the transport characteristics of higher plants.     

The role of arctic zooplankton in biogeochemical cycles: respiration and excretion of ammonia and phosphate during summer

The study of the structural and functional properties of key components of polar marine ecosystems has received increased attention in order to better understand the ecological consequences of future sea temperature rise and seasonal ice retraction. Owing to this purpose, during the ATOS-Arctic cruise, held in July 2007 in the framework of the 2007–2008 International Polar Year, we studied the respiratory carbon demand of mesozooplankton as well as their contribution to the regeneration of inorganic nitrogen and phosphorus (NH₄-N and PO₄-P) via excretion. The studied area comprised several stations along a latitudinal gradient in the East Greenland current, plus a network of stations NW of the Svalbard islands. The specific respiratory carbon losses and phosphorus (PO₄-P) excretion rates were similar or slightly higher than some reports for Arctic mesozooplankton, but the nitrogen (NH₄-N) excretion rates were higher by a factor of 3 when compared with previous data sets. The mesozooplankton respiratory losses were equivalent to 23% of primary production, and at turn zooplankton contributed by excretion to more than 50% of the N and P required by phytoplankton. Although C:N, C:P and N:P metabolic atomic quotients almost coincided with the average Redfield’s stoichiometric ratios, the low C:N values when compared to previous reports suggested a predominance of protein-related metabolic substrates. The potential consequences of changes observed in the C:N, N:P and C:P metabolic ratios of mesozooplankton for Arctic marine ecosystems are discussed.     

Water pulses and biogeochemical cycles in arid and semiarid ecosystems

The episodic nature of water availability in arid and semiarid ecosystems has significant consequences on belowground carbon and nutrient cycling. Pulsed water events directly control belowground processes through soil wet-dry cycles. Rapid soil microbial response to incident moisture availability often results in almost instantaneous C and N mineralization, followed by shifts in C/N of microbially available substrate, and an offset in the balance between nutrient immobilization and mineralization. Nitrogen inputs from biological soil crusts are also highly sensitive to pulsed rain events, and nitrogen losses, particularly gaseous losses due to denitrification and nitrate leaching, are tightly linked to pulses of water availability. The magnitude of the effect of water pulses on carbon and nutrient pools, however, depends on the distribution of resource availability and soil organisms, both of which are strongly affected by the spatial and temporal heterogeneity of vegetation cover, topographic position and soil texture. The inverse texture hypothesis for net primary production in water-limited ecosystems suggests that coarse-textured soils have higher NPP than fine-textured soils in very arid zones due to reduced evaporative losses, while NPP is greater in fine-textured soils in higher rainfall ecosystems due to increased water-holding capacity. With respect to belowground processes, fine-textured soils tend to have higher water-holding capacity and labile C and N pools than coarse-textured soils, and often show a much greater flush of N mineralization. The result of the interaction of texture and pulsed rainfall events suggests a corollary hypothesis for nutrient turnover in arid and semiarid ecosystems with a linear increase of N mineralization in coarse-textured soils, but a saturating response for fine-textured soils due to the importance of soil C and N pools. Seasonal distribution of water pulses can lead to the accumulation of mineral N in the dry season, decoupling resource supply and microbial and plant demand, and resulting in increased losses via other pathways and reduction in overall soil nutrient pools. The asynchrony of resource availability, particularly nitrogen versus water due to pulsed water events, may be central to understanding the consequences for ecosystem nutrient retention and long-term effects on carbon and nutrient pools. Finally, global change effects due to changes in the nature and size of pulsed water events and increased asynchrony of water availability and growing season will likely have impacts on biogeochemical cycling in water-limited ecosystems.     

Transpiration of trees and forest stands: short and long-term monitoring using sapflow methods

We show that sapflow is a useful tool for studies of water fluxes in forest ecosystems, because (i) it gives access to the spatial variability within a forest stand, (ii) it can be used even on steep slopes, and (iii) when combined with eddy correlation measurements over forests, it allows separation of individual tree transpiration from the total water loss of the stand. Moreover, sapflow techniques are quite easy to implement. Four sapflow techniques currently coexist, all based on heat diffusion in the xylem. We found a good agreement between three of these techniques. Most results presented here were obtained using the radial flow meter (Granier 1985). Tree sapflow is computed as sap flux density times sapwood area. To scale up from trees to a stand, measurements have to be made on a representative sample of trees. Thus, a number of trees in each circumference class is selected according to the fraction of sapwood they represent in the total sapwood area of the stand. The variability of sap flux density among trees is usually low (CV. 10–15%) in close stands of temperate coniferous or deciduous forests, but is much higher (35–50%) in a tropical rain forest. It also increases after thinning or during a dry spell. A set of 5–10 sapflow sensors usually provides an accurate estimate of stand transpiration. Transpiration measured on two dense spruce stands in the Vosges mountains (France) and one Scot's pine plantation in the Rhine valley (Germany) showed that maximum rate was related to stand LAI and to local climate. Preliminary results comparing the sapflow of a stand of Pinus banksiana to the transpiration of large branches, as part of the BOREAS programme in Saskachewan, Canada showed a similar trend. For modelling purposes, tree canopy conductance (g_c) was calculated from Penman-Monteith equation. In most experiments, calculated canopy conductance was dependent on global radiation (positive effect) and on vapour pressure deficit (negative effect) in the absence of other limiting factors. A comparison of the vapour pressure deficit response curves of g_c for several tree species and sites showed only small differences among spruce, oak and pine forests when including understorey. Tropical rainforests exhibited a similar behaviour.     

Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plant water potential in Neotropical savanna trees

Seasonal regulation of leaf water potential (_L) was studied in eight dominant woody savanna species growing in Brazilian savanna (Cerrado) sites that experience a 5-month dry season. Despite marked seasonal variation in precipitation and air saturation deficit (D), seasonal differences in midday minimum _L were small in all of the study species. Water use and water status were regulated by a combination of plant physiological and architectural traits. Despite a nearly 3-fold increase in mean D between the wet and dry season, a sharp decline in stomatal conductance with increasing D constrained seasonal variation in minimum _L by limiting transpiration per unit leaf area (E). The leaf surface area per unit of sapwood area (LA/SA), a plant architectural index of potential constraints on water supply in relation to transpirational demand, was about 1.5–8 times greater in the wet season compared to the dry season for most of the species. The changes in LA/SA from the wet to the dry season resulted from a reduction in total leaf surface area per plant, which maintained or increased total leaf-specific hydraulic conductance (G_t) during the dry season. The isohydric behavior of Cerrado tree species with respect to minimum _L throughout the year thus was the result of strong stomatal control of evaporative losses, a decrease in total leaf surface area per tree during the dry season, an increase in total leaf-specific hydraulic conductance, and a tight coordination between gas and liquid phase conductance. In contrast with the seasonal isohydric behavior of minimum _L, predawn _L in all species was substantially lower during the dry season compared to the wet season. During the dry season, predawn _L was more negative than bulk soil estimated by extrapolating plots of E versus _L to E=0. Predawn disequilibrium between plant and soil was attributable largely to nocturnal transpiration, which ranged from 15 to 22% of the daily total. High nocturnal water loss may also have prevented internal water storage compartments from being completely refilled at night before the onset of transpiration early in the day.     

Malate plays a central role in plant nutrition

Malate occupies a central role in plant metabolism. Its importance in plant mineral nutrition is reflected by the role it plays in symbiotic nitrogen fixation, phosphorus acquisition, and aluminum tolerance. In nitrogen-fixing root nodules, malate is the primary substrate for bacteroid respiration, thus fueling nitrogenase. Malate also provides the carbon skeletons for assimilation of fixed nitrogen into amino acids. During phosphorus deficiency, malate is frequently secreted from roots to release unavailable forms of phosphorus. Malate is also involved with plant adaptation to aluminum toxicity. To define the genetic and biochemical regulation of malate formation in plant nutrition we have isolated and characterized genes involved in malate metabolism from nitrogen-fixing root nodules of alfalfa and those involved in organic acid excretion from phosphorus-deficient proteoid roots of white lupin. Moreover, we have overexpressed malate dehydrogenase in alfalfa in attempts to improve nutrient acquisition. This report is an overview of our efforts to understand and modify malate metabolism, particularly in the legumes alfalfa and white lupin.     

Stomata response to changes in temperature and humidity in wheat cultivars grown under contrasting climatic conditions

Stomatal response to changes in temperature and humidity was studied in wheat (Triticum aestivum L.) cv. Iren’ cultivated under conditions of high water supply and cv. Kazakhstanskaya 10, which is relatively drought tolerant. Experiments were performed under both laboratory and field conditions. It was demonstrated that stomata of cv. Kazakhstanskaya 10 plants closed rapidly with reducing humidity (the response of the first type), whereas, in cv. Iren’, this response was less expressed and, under conditions of a high water content in soil, stomatal conductance could increase in response to reduced humidity (the response of the second type). At an increased stomatal conductance and transpiration, water content in cv. Iren’ plants was maintained due to the increase in hydraulic conductance and water inflow from the roots. A possible role of the first-type response (rapid stomata closure) for growth maintenance under drought and of the second-type response (a parallel increase in the stomatal and hydraulic conductance) for providing of rapid growth and high productivity under sufficient water supply is discussed. A possibility to use the type of stomata behavior for cultivar assessment is considered.     

Furan fatty acids: their role in plant systems

Furan fatty acids (F-acids) are heterocyclic fatty acids having a furan ring in their structure. Most existing studies on F-acids are related to either fish or other marine animals. Even though F-acids have been detected in many plant species, not much work has been done exclusively in plants of economic importance, especially oilseed crops. This review focuses mainly on the functions and roles of F-acids in plants. In plants, they are bound to phospholipids by substituting PUFA and function as free radical scavengers suggesting their role in defense against oxidative stress. Owing to their antioxidative property F-acids are highly unstable and their photooxidative products can contribute to the flavor of edible oils.     

Access and excess problems in plant nutrition

As plant nutrition issues are redefined by society, new applications emerge for a basic understanding of nutrient use efficiency in soil-plant processes to avoid excess on rich soils as commonly found in the temperate zone and make the best of it under access-limited conditions common in the tropics. The main challenge of plant nutrition may be to increase the width of the domain between the access and excess frontiers, rather than to define a single `economic optimum' point. Two approaches are discussed to widen this domain: the technical paradigm of precision farming and the ecological analogue approach based on filter functions and complementarity of components in mixed plant systems. Current understanding of plant nutrition, largely focused on monocultural situations, needs to be augmented by the interactions that occur in more complex systems, including agroforestry and intercropping as these may form part of the answer in both the excess and shortage type of situation. Simulations with the WaNuLCAS model to explore the concepts of a 'safety-net' for mobile nutrients by deep rooted plants suggested a limited but real opportunity to intercept nutrients on their way out of the system and thus increase nutrient use-efficiency at the system level. The impacts of rhizosphere modification to mobilize nutrients in mixed-species systems were shown to depend on the degree of synlocation of roots of the various plant components, as well as on the long-term replenishment of the nutrient resources accessed. In conclusion, the concepts and tools to help farmers navigate between the scylla of access and the charibdis of excess problems in plant nutrition certainly exist, but their use requires an appreciation of the site-specific interactions and various levels of internal regulation, rather than a reliance alone on genetic modification of plants aimed at transferring specific mechanisms out of context.     

Restriction of transpiration rate under high vapour pressure deficit and non‐limiting water conditions is important for terminal drought tolerance in cowpea

Drought stress is a major constraint on cowpea productivity, since the crop is grown under warm conditions on sandy soils having low water‐holding capacity. For enhanced performance of crops facing terminal drought stress, like cowpea, water‐saving strategies are crucial. In this work, the growth and transpiration rate (TR) of 40 cowpea genotypes with contrasting response to terminal drought were measured under well‐watered conditions across different vapour pressure deficits (VPD) to investigate whether tolerant and sensitive genotypes differ in their control of leaf water loss. A method is presented to indirectly assess TR through canopy temperature (CT) and the index of canopy conductance (Ig). Overall, plants developed larger leaf area under low than under high VPD, and there was a consistent trend of lower plant biomass in tolerant genotypes. Substantial differences were recorded among genotypes in TR response to VPD, with tolerant genotypes having significantly lower TR than sensitive ones, especially at times with the highest VPD. Genotypes differed in TR response to increasing VPD, with some tolerant genotypes exhibiting a clear VPD breakpoint at about 2.25 kPa, above which there was very little increase in TR. In contrast, sensitive genotypes presented a linear increase in TR as VPD increased, and the same pattern was found in some tolerant lines, but with a smaller slope. CT, estimated with thermal imagery, correlated well with TR and Ig and could therefore be used as proxy for TR. These results indicate that control of water loss discriminated between tolerant and sensitive genotypes and may, therefore, be a reliable indicator of terminal drought stress tolerance. The water‐saving characteristics of some genotypes are hypothesised to leave more soil water for pod filling, which is crucial for terminal drought adaptation.