Iron Uptake and Homeostasis in Microorganisms

Preface. Iron is considered to be a minor element employed, in a variety of forms, by nearly all living organisms. In some cases, it is utilised in large quantities, for instance for the formation of magnetosomes within magnetotactic bacteria or during use of iron as a respiratory donor or acceptor by iron oxidising or reducing bacteria. However, in most cases the role of iron is restricted to its use as a cofactor or prosthetic group assisting the biological activity of many different types of protein. The key metabolic processes that are dependent on iron as a cofactor are numerous; they include respiration, light harvesting, nitrogen fixation, the Krebs cycle, redox stress resistance, amino acid synthesis and oxygen transport. Indeed, it is clear that Life in its current form would be impossible in the absence of iron. One of the main reasons for the reliance of Life upon this metal is the ability of iron to exist in multiple redox states, in particular the relatively stable ferrous (Fe2+) and ferric (Fe3+) forms. The availability of these stable oxidation states allows iron to engage in redox reactions over a wide range of midpoint potentials, depending on the coordination environment, making it an extremely adaptable mediator of electron exchange processes. Iron is also one of the most common elements within the Earth’s crust (5% abundance) and thus is considered to have been readily available when Life evolved on our early, anaerobic planet. However, as oxygen accumulated (the ‘Great oxidation event’) within the atmosphere some 2.4 billion years ago, and as the oceans became less acidic, the iron within primordial oceans was converted from its soluble reduced form to its weakly-soluble oxidised ferric form, which precipitated (~1.8 billion years ago) to form the ‘banded iron formations’ (BIFs) observed today in Precambrian sedimentary rocks around the world. These BIFs provide a geological record marking a transition point away from the ancient anaerobic world towards modern aerobic Earth. They also indicate a period over which the bio-availability of iron shifted from abundance to limitation, a condition that extends to the modern day. Thus, it is considered likely that the vast majority of extant organisms face the common problem of securing sufficient iron from their environment – a problem that Life on Earth has had to cope with for some 2 billion years. This struggle for iron is exemplified by the competition for this metal amongst co-habiting microorganisms who resort to stealing (pirating) each others iron supplies! The reliance of micro-organisms upon iron can be disadvantageous to them, and to our innate immune system it represents a chink in the microbial armour, offering an opportunity that can be exploited to ward off pathogenic invaders. In order to infect body tissues and cause disease, pathogens must secure all their iron from the host. To fight such infections, the host specifically withdraws available iron through the action of various iron depleting processes (e.g. the release of lactoferrin and lipocalin-2) – this represents an important strategy in our defence against disease. However, pathogens are frequently able to deploy iron acquisition systems that target host iron sources such as transferrin, lactoferrin and hemoproteins, and thus counteract the iron-withdrawal approaches of the host. Inactivation of such host-targeting iron-uptake systems often attenuates the pathogenicity of the invading microbe, illustrating the importance of ‘the battle for iron’ in the infection process. The role of iron sequestration systems in facilitating microbial infections has been a major driving force in research aimed at unravelling the complexities of microbial iron transport processes. But also, the intricacy of such systems offers a challenge that stimulates the curiosity. One such challenge is to understand how balanced levels of free iron within the cytosol are achieved in a way that avoids toxicity whilst providing sufficient levels for metabolic purposes – this is a requirement that all organisms have to meet. Although the systems involved in achieving this balance can be highly variable amongst different microorganisms, the overall strategy is common. On a coarse level, the homeostatic control of cellular iron is maintained through strict control of the uptake, storage and utilisation of available iron, and is co-ordinated by integrated iron-regulatory networks. However, much yet remains to be discovered concerning the fine details of these different iron regulatory processes. As already indicated, perhaps the most difficult task in maintaining iron homeostasis is simply the procurement of sufficient iron from external sources. The importance of this problem is demonstrated by the plethora of distinct iron transporters often found within a single bacterium, each targeting different forms (complex or redox state) of iron or a different environmental condition. Thus, microbes devote considerable cellular resource to securing iron from their surroundings, reflecting how successful acquisition of iron can be crucial in the competition for survival. The aim of this book is provide the reader with an overview of iron transport processes within a range of microorganisms and to provide an indication of how microbial iron levels are controlled. This aim is promoted through the inclusion of expert reviews on several well studied examples that illustrate the current state of play concerning our comprehension of how iron is translocated into the bacterial (or fungal) cell and how iron homeostasis is controlled within microbes. The first two chapters (1-2) consider the general properties of microbial iron-chelating compounds (known as ‘siderophores’), and the mechanisms used by bacteria to acquire haem and utilise it as an iron source. The following twelve chapters (3-14) focus on specific types of microorganism that are of key interest, covering both an array of pathogens for humans, animals and plants (e.g. species of Bordetella, Shigella, , Erwinia, Vibrio, Aeromonas, Francisella, Campylobacter and Staphylococci, and EHEC) as well as a number of prominent non-pathogens (e.g. the rhizobia, E. coli K-12, Bacteroides spp., cyanobacteria, Bacillus spp. and yeasts). The chapters relay the common themes in microbial iron uptake approaches (e.g. the use of siderophores, TonB-dependent transporters, and ABC transport systems), but also highlight many distinctions (such as use of different types iron regulator and the impact of the presence/absence of a cell wall) in the strategies employed. We hope that those both within and outside the field will find this book useful, stimulating and interesting. We intend that it will provide a source for reference that will assist relevant researchers and provide an entry point for those initiating their studies within this subject. Finally, it is important that we acknowledge and thank wholeheartedly the many contributors who have provided the 14 excellent chapters from which this book is composed. Without their considerable efforts, this book, and the understanding that it relays, would not have been possible. Simon C Andrews and Pierre Cornelis

Observations and modeling of banded orographic convection

Radar images and numerical simulations of three shallow convective precipitation events over the Coastal Range in western Oregon are presented. In one of these events, unusually well-defined quasi-stationary banded formations produced large precipitation enhancements in favored locations, while varying degrees of band organization and lighter precipitation accumulations occurred in the other two cases. The difference between the more banded and cellular cases appeared to depend on the vertical shear within the orographic cap cloud and the susceptibility of the flow to convection upstream of the mountain. Numerical simulations showed that the rainbands, which appeared to be shear-parallel convective roll circulations that formed within the unstable orographic cap cloud, developed even over smooth mountains. However, these banded structures were better organized, more stationary, and produced greater precipitation enhancement over mountains with small-scale topographic obstacles. Low-amplitude random topographic roughness elements were found to be just as effective as more prominent subrange-scale peaks at organizing and fixing the location of the orographic rainbands.

Dynamics of convectively driven banded jets in the laboratory

The banded organization of clouds and zonal winds in the atmospheres of the outer planets has long fascinated observers. Several recent studies in the theory and idealized modeling of geostrophic turbulence have suggested possible explanations for the emergence of such organized patterns, typically involving highly anisotropic exchanges of kinetic energy and vorticity within the dissipationless inertial ranges of turbulent flows dominated (at least at large scales) by ensembles of propagating Rossby waves. The results from an attempt to reproduce such conditions in the laboratory are presented here. Achievement of a distinct inertial range turns out to require an experiment on the largest feasible scale. Deep, rotating convection on small horizontal scales was induced by gently and continuously spraying dense, salty water onto the free surface of the 13-m-diameter cylindrical tank on the Coriolis platform in Grenoble, France. A “planetary vorticity gradient” or “β effect” was obtained by use of a conically sloping bottom and the whole tank rotated at angular speeds up to 0.15 rad s−1. Over a period of several hours, a highly barotropic, zonally banded large-scale flow pattern was seen to emerge with up to 5–6 narrow, alternating, zonally aligned jets across the tank, indicating the development of an anisotropic field of geostrophic turbulence. Using particle image velocimetry (PIV) techniques, zonal jets are shown to have arisen from nonlinear interactions between barotropic eddies on a scale comparable to either a Rhines or “frictional” wavelength, which scales roughly as (β/Urms)−1/2. This resulted in an anisotropic kinetic energy spectrum with a significantly steeper slope with wavenumber k for the zonal flow than for the nonzonal eddies, which largely follows the classical Kolmogorov k−5/3 inertial range. Potential vorticity fields show evidence of Rossby wave breaking and the presence of a “hyperstaircase” with radius, indicating instantaneous flows that are supercritical with respect to the Rayleigh–Kuo instability criterion and in a state of “barotropic adjustment.” The implications of these results are discussed in light of zonal jets observed in planetary atmospheres and, most recently, in the terrestrial oceans.

The impact of deformation strain on the formation of banded clouds in idealized modeling experiments

Experiments are performed using an idealized version of an operational forecast model to determine the impact on banded frontal clouds of the strength of deformational forcing, low-level baroclinicity, and model representation of convection. Line convection is initiated along the front, and slantwise bands extend from the top of the line-convection elements into the cold air. This banding is attributed primarily to M adjustment. The cross-frontal spreading of the cold pool generated by the line convection leads to further triggering of upright convection in the cold air that feeds into these slantwise bands. Secondary low-level bands form later in the simulations; these are attributed to the release of conditional symmetric instability. Enhanced deformation strain leads to earlier onset of convection and more coherent line convection. A stronger cold pool is generated, but its speed is reduced relative to that seen in experiments with weaker deformational strain, because of inhibition by the strain field. Enhanced low-level baroclinicity leads to the generation of more inertial instability by line convection (for a given capping height of convection), and consequently greater strength of the slantwise circulations formed by M adjustment. These conclusions are based on experiments without a convective-parametrization scheme. Experiments using the standard or a modified scheme for this model demonstrate known problems with the use of this scheme at the awkward 4 km grid length used in these simulations. Copyright © 2008 Royal Meteorological Society

Jupiter's and Saturn's convectively driven banded jets in the laboratory

The banded patterns of cloud and wind are among the most striking features of the atmospheres of Jupiter and Saturn, but their dynamical origin remains poorly understood. Most approaches towards understanding zonation so far (also in the terrestrial oceans) have used highly idealized models to show that it might originate from dynamical anisotropy in a shallow turbulent fluid layer due to the planetary β-effect. Here we report the results of laboratory experiments, conducted on a 14-m diameter turntable, which quantitatively confirm that multiple zonal jets may indeed be generated and maintained by this mechanism in the presence of deep convection and a topographic β-effect. At the very small values of Ekman number (≤2 × 10−5) and large local Reynolds numbers (≥2000, based on jet scales) achieved, the kinetic energy spectra suggest the presence of both energy-cascading and enstrophy-cascading inertial ranges in addition to the zonation near twice the Rhines wave number.

Field trials to assess the uptake of arsenic by vegetables from contaminated soils and soil remediation with iron oxides

The uptake of arsenic (As) by plants from contaminated soils presents a health hazard that may affect the use of agricultural and former industrial land. Methods for limiting the hazard are desirable. A proposed remediation treatment comprises the precipitation of iron (Fe) oxides in the contaminated soil by adding ferrous sulfate and lime. The effects on As bioavailability were assessed using a range of vegetable crops grown in the field. Four UK locations were used, where soil was contaminated by As from different sources. At the most contaminated site, a clay loam containing a mean of 748 mg As kg(-1) soil, beetroot, calabrese, cauliflower, lettuce, potato, radish and spinach were grown. For all crops except spinach, ferrous sulfate treatment caused a significant reduction in the bioavailability of As in some part of the crop. Application of ferrous sulfate in solution, providing 0.2% Fe oxides in the soil (0-10 cm), reduced As uptake by a mean of 22%. Solid ferrous sulfate was applied to give concentrations of 0.5% and 1% Fe oxides: the 0.5% concentration reduced As uptake by a mean of 32% and the 1% concentration gave no significant additional benefit. On a sandy loam containing 65 mg As kg(-1) soil, there was tentative evidence that ferrous sulfate treatment up to 2% Fe oxides caused a significant reduction in lettuce As, but calabrese did not respond. At the other two sites, the effects of ferrous sulfate treatment were not significant, but the uptake of soil As was low in treated and untreated soils. Differences between sites in the bioavailable fraction of soil As may be related to the soil texture or the source of As. The highest bioavailability was found on the soil which had been contaminated by aerial deposition and had a high sand content. (C) 2003 Elsevier Science B.V. All rights reserved.

Spectral properties, iron oxide content and provenance of Namib dune sands

This paper applies multispectral remote sensing techniques to map the Fe-oxide content over the entire Namib sand sea. Spectrometric analysis is applied to field samples to identify the reflectance properties of the dune sands which enable remotely sensed Fe-oxide mapping. The results indicate that the pattern of dune colour in the Namib sand sea arises from the mixing of at least two distinct sources of sand; a red component of high Fe-oxide content (present as a coating on the sand grains) which derives from the inland regions, particularly from major embayments into the Southern African escarpment; and a yellow coastal component of low Fe-oxide content which is brought into the area by northward-moving aeolian transport processes. These major provenances are separated by a mixing zone between 20 kin and 90 kin from the coast throughout the entire length of the sand sea. Previous workers have also recognised a third, fluvial, provenance, but the methodology applied here is not able to map this source as a distinct spectral component. (c) 2006 Elsevier B.V. All rights reserved.

Granulometric characterization and evaluation of annually banded mid-Holocene estuarine silts, Welsh Severn Estuary (UK): coastal change, sea level and climate

Holocene silts (salt marshes) and highest intertidal-supratidal peats are superbly exposed on a 15 kin coastal transect which reveals two laterally extensive units of annually banded silts (Beds 3, 7) associated with three transgressive-regressive silt-peat cycles (early sixth-early fourth millennium BC). Bed 3 in places is concordantly and gradationally related to peats above and below, but in others transgresses older strata. Bed 7 also grades up into peat, but everywhere overlies a discordance. The banding in Bed 3 at three main and two minor sites was resolved and characterized texturally at high-resolution (2.5/5 mm contiguous slices) using laser granulometry (LS230 with PIDS) and a comprehensive scheme of data-assessment. Most of Bed 3 formed very rapidly, at peak values of several tens of millimetres annually, in accordance with modelled effects of sea-level fluctuations on mature marshes (bed concordant and gradational) and on marshes growing up after coastal erosion and retreat (bed with discordant base). Using data from the modern Severn Estuary, the textural contrast within bands, and its variation between bands, points to a variable but overall milder mid-Holocene climate than today. The inter-annual variability affected marsh dynamics, as shown by the behaviour of the finely divided plant tissues present. Given local calibration, the methodology is applicable to other tidal systems with banded silts in Britain and mainland northwest Europe. (c) 2006 Elsevier Ltd. All rights reserved.

Dust production and the release of iron oxides resulting from the aeolian abrasion of natural dune sands

Global dust trajectories indicate that significant quantities of aeolian-transported iron oxides originate in contemporary dryland areas. One potential source is the iron-rich clay coatings that characterize many sand-sized particles in desert dunefields. This paper uses laboratory experiments to determine the rate at which these coatings can be removed from dune sands by aeolian abrasion. The coatings impart a red colour to the grains to which previous researchers have assigned variable geomorphological significance. The quantities or iron removed during a 120 hour abrasion experiment are small (99 mg kg(-1)) and difficult to detect by eye; however, high resolution spectroscopy clearly indicates that ferric oxides are released during abrasion and the reflectance of the particles alters. One of the products of aeolian abrasion is fine particles (<10 mum diameter) with the potential for long distance transport. Copyright (C) 2004 John Wiley Sons, Ltd.

Seasonal deposition of Holocene banded sediments in the Severn Estuary Levels (southwest Britain): palynological and sedimentological evidence

Banded sediments outcrop widely in the intertidal zone of the Severn Estuary and have been suggested, on the basis of textural analysis, to have formed in response to seasonal variations in sea temperature and windiness (Holocene, 14 (2004) 536). Here palynological and sedimentological analyses of banded sediments of mid-Holocene date from Gold Cliff, on the Welsh side of the Severn Estuary, are combined to test and further develop the hypothesis of seasonal deposition. Pollen percentage and concentration data are presented from a short sequence of bands to establish whether textural variations in the bands coincide with variations in pollen content reflecting seasonal flowering patterns. It is shown that fine-grained band parts contain higher total pollen concentrations, and a higher proportion of pollen from late spring- to summer-flowering plants, than coarse-grained band parts. Pollen in the coarser deposits appears primarily to reflect deposition from the buffering `reservoir' of suspended pollen in the estuarine water-body and from rivers, when there is little pollen in the air in winter, while the finer sediments contain pollen deposited from the atmosphere during the flowering season, superimposed on these `background' sources. The potential of such deposits for refining chronologies and identifying seasonality of coastal processes is noted, and the results of charcoal particle analysis of the bands presented as an example of how they have the potential to shed light on seasonal and annual patterns of human activity. (C) 2004 Elsevier Ltd. All rights reserved.