Introduction

Fundamentally, biogeochemical cycling involves the transformation of compounds between various forms, and a movement of such compounds within and between compartments of the biosphere and geosphere. These processes operate across a wide range of spatial and temporal scales, from micrometres to kilometres, from seconds to centuries. In terrestrial systems, transformations and movement of materials below-ground are governed by the spatial organization of the soil system, and particularly the architecture of the pore network. This ‘inner space’ provides the physical framework in and through which the majority of soil-based processes occur. The labyrinthine nature of the pore network, and the exchange properties of associated surfaces, strongly modulates the transport of materials through the soil matrix. From a physicochemical perspective soil structure generally retards transport processes for two main reasons: the complex geometry of the pore network increases path lengths, both for diffusive and bulk-flow movement; and charged mineral and organic constituents in the soil act as exchange surfaces which bind transportable compounds to varying degrees. Transport processes may also be accelerated by structural properties, for example if solutes or particulates are carried via preferential and bypass-flow channels of water through macropores.

Soil organisms play a key role in driving terrestrial nutrient cycling, and play both direct and indirect roles in effecting and affecting transport processes. Fungi contribute a particularly wide range of functions relating to nutrient cycling.

Introduction

This chapter reviews the distribution, mechanism and impact of mineral tunnelling by soil ectomycorrhizal fungi (EMF). Most trees in boreal forests live in close relation with EMF (Smith & Read, 1997). These EMF mediate nutrient uptake; they form an extension of the tree roots. In turn they obtain carbohydrates from the tree. Over the years ectomycorrhizal (EM) research has a strong focus on nutrient acquisition by EMF from organic sources (Read, 1991). In boreal forest systems, however, minerals could also be an important nutrient source, especially for calcium, potassium and phosphorus (Likens et al., 1994, 1998; Blum et al., 2002). Recent developments in EM research suppose a role for EMF in mobilizing nutrients from minerals (see Wallander, Chapter 14, this volume).

In 1997, Jongmans et al. described small tunnel-like features in feldspar and hornblende grains from Swedish forest soils. These tunnels have the shape of fungal hyphae: a constant width between 3 and 10 μm, smooth borders and a rounded end. In that way they differ from other weathering phenomena such as etch pitches and cracks (Fig. 13.1). In some tunnels hyphae were found. Jongmans et al. (1997) postulated that EMF created these tunnels by mineral dissolution through the exudation of low-molecular-weight organic compounds and subsequent removal of the weathering products. The weathering products like calcium, magnesium and potassium are supposed to be transported to the tree roots. In this way the host tree has direct access to mineral-bound nutrients, bypassing the bulk soil solution (van Breemen et al., 2000a; Landeweert et al., 2001).

Introduction

The first aim of this chapter is to summarise the biochemical basis of photosynthesis in planktic algae and to review the physiological sensitivities of carbon fixation and assimilation under the environmental conditions experienced by natural populations of phytoplankton. These fundamental aspects of autotrophy are plainly relevant to the dynamics and population ecology of individual algal species, functioning within the constraints set by temperature and by the natural fluxes of light energy and inorganic carbon. They are also relevant to the function of entire pelagic systems as, frequently, they furnish the major source of energy, in the form of reduced carbon, to heterotrophic consumers. The yields of fish, birds and mammals in aquatic systems are ultimately related to the harvestable and assimilable sources of carbon bonds. In turn, the energy and resource fluxes through the entire biosphere are greatly influenced by pelagic primary producers, impinging on the gaseous composition of the atmosphere and the heat balance of the whole planet.

Here, we shall be concerned with events at the population, community and ecosystem levels. However, it is necessary to emphasise at the start of the chapter that recent advances in understanding of planetary carbon stores and fluxes assist our appreciation of the relative global importance of aquatic photosynthesis. To those biologists of my generation brought up with the exclusive axiom that animals derive their energy by respiring (oxidising) the carbohydrates and proteins manufactured (reduced) by photosynthesising plants, the presently perceived realities of aquatic-reductant fluxes may seem quite counter-intuitive.

Introduction

Although fungi are generally disregarded in the biogeochemical literature, they undoubtedly constitute crucial biogeochemical factors in many elemental cycles. This fact, combined with their abundance in the soil, warrants greater detailed study into their geoecological impact. The network formed by fungal filaments can represent 10 000 km of thread-like mycelia in 1 m2 of fertile soil. Their mass is evaluated at 3500 kg ha− 1 at a depth of 20 cm in an average continental soil, i.e. taking into account all the different terrestrial environments on Earth (Gobat et al., 2004). In comparison, bacteria and algae would represent 1500 and 10–1000 kg ha− 1 respectively, in the same virtual average soil. Fungi are not only biologically important as saprophytes in the recycling of organic matter, but also play a geological role by excreting notable amounts of organic acids, among which oxalic acid is particularly important (Gadd, 1999), contributing to continental weathering as well as to mineral neogenesis (Verrecchia & Dumont, 1996; Verrecchia, 2000; Burford et al., 2003 a, b).

The first fossil fungi have been identified in rocks dated from the Ordovician, i.e. 460 to 455 Ma ago (Redecker et al., 2000). However, molecular clock estimates for the evolution of fungi have suggested a Late Precambrian (600 Ma) colonization on land (Berbee & Taylor 2000). Recent molecular studies, based on protein sequence analysis, indicate that fungi were present on continents 1 billion years ago and possibly affected (together with plants) the evolution of Earth's atmosphere and climate since 700 Ma (Heckman et al., 2001).

Introduction

Exploration of the microbial world got off to a slow start some 350 years ago, when Leeuwenhoek and his contemporaries focused their microscopes on very small life forms. It was not until about 20 years ago, however, that exploration of the world of intra-terrestrial microbes gathered momentum. Until then, it was generally assumed that life could not persist deep underground, out of reach of the sun and a photosynthetic ecosystem base. In the mid 1980s, the drilling of deep holes for scientific research started. Holes up to thousands of metres deep were drilled in hard as well as sedimentary rock, and up came microbes in numbers equivalent to what could be found in many surface ecosystems (Pedersen, 1993). The deep subterranean biosphere had been discovered.

Defining the boundary between the ground-surface biosphere and the subterranean biosphere is problematic: various scientists define it differently, and there is no general consensus. For our purposes the main criterion is that the subterranean biosphere begins where contact with the surface biosphere is lost. This lies beneath soil and root zones, beneath the ground-water table, and beneath sediment and crust surfaces. A long time should have elapsed since last surface contact, ‘long time’ in this respect being at least several decades, preferably hundreds of years or more. In our view it is not depth per se that defines a subterranean ecosystem; rather, it is the duration of isolation from the surface.

Introduction

Mycorrhizal fungi play a central role in biogeochemical cycles since they obtain carbon from their photosynthetic plant hosts and allocate this via their mycelia to the soil ecosystem. The mycelia interact with a range of organic and inorganic substrates, as well as with different organisms such as bacteria, fungi, soil micro- and meso-fauna and the roots of secondary hosts or non-host plants. Some of the carbon allocated to the mycelium is used to make compounds such as enzymes, organic acids, siderophores or antibiotics, which influence biotic or abiotic substrates through processes such as decomposition, weathering or antibiosis. Organic and inorganic nutrients mobilized from these substrates can be taken up by the mycorrhizal mycelia and translocated to their plant hosts, influencing plant growth, community structure and vegetation dynamics. Ultimately these changes have further impacts on biogeochemical cycles. Different types of mycorrhizal symbiosis have evolved as adaptations to different suites of edaphic parameters, resulting in the characteristic vegetation types that dominate different terrestrial biomes. Other chapters in this book consider specific contributions of ectomycorrhizal fungi to mineral dissolution (see Wallander, Chapter 14, this volume), carbon and nitrogen cycling (see Hobbie & Wallander, Chapter 5, this volume) and mineral tunnelling (see Smits, Chapter 13, this volume). In this chapter we concentrate on how these activities are integrated and on ways in which ectomycorrhizal hyphae may interact with other microorganisms to influence biogeochemical cycles.

Introduction

Arbuscular mycorrhizal fungi (AMF) are the most ancient, widespread and ubiquitous of all the groups of mycorrhiza: they have a global distribution in widely contrasting plant communities including the Tropics, the Boreal forest, arctic tundra and all types of grassland. Considerable effort has been made in recent years in order to set AMF within a robust phylogeny. Recent advances in molecular biological techniques have enabled scientists to place AMF in a new division, the Glomeromycota. At present, this division contains only about 150 species, which is remarkable given the enormous number of plant species the fungi readily colonize. The mutualistic symbioses that AMF form with their host plants give rise to a number of important benefits to both the plant and fungus. A brief glance at a standard mycorrhizal text will list many ecologically important attributes, such as improved disease resistance, water uptake, nutrient transfer and the ability of the fungus to be a major sink for photosynthate. Indeed, the importance of AMF for nutrient uptake and carbon allocation has been recognized for decades. The ability of AMF (and other mycorrhizal types) to utilize recent plant photosynthate and thus have access to a near continuous supply of energy immediately gives them a potential advantage over saprotrophic micro-organisms, which are forced to obtain their energy in the highly carbon-limited heterogeneous soil environment.

In praise of geomycology

Interactions between the microbially dominated biosphere and the geosphere have and are profoundly affecting our planet and all life on it. Geomicrobiology can be defined as the study of the role that microbes have played and are playing in processes of fundamental importance to geology, and within the diffuse boundaries enclosed by this definition, fungi are important components. Some of the major geological processes affected by microbial activities include mineral formation, mineral degradation (including weathering, bioleaching, soil and sediment formation), element cycling and fossil fuel genesis and degradation. The cycling of component elements from organic and inorganic substrates as a result of these processes can be termed biogeochemical cycling, which again emphasizes the interplay between physicochemical and biological mechanisms. The study of the roles and importance of fungi as agents of geological change can be termed geomycology and fungi are ideally suited for this purpose. The branching, filamentous mode of growth allows efficient colonization and exploration of solid substrates while extracellular release of enzymes and other metabolites mediates many organic and inorganic transformations. Considerable physical force can arise from hyphal penetration while translocation of resources through the mycelium enables exploitation of environments where nutrients have an irregular distribution. Fungi can attack silicates, carbonates, phosphates and other minerals while their carbonaceous predilections are well-known, extending to recalcitrant organic molecules of natural origin, e.g. lignin and chitin, or from anthropogenic activity, e.g. pesticides and other xenobiotics.

Introduction

Fungi are chemoheterotrophic organisms, ubiquitous in subaerial and subsoil environments, and important as decomposers, animal and plant symbionts and pathogens, and spoilage organisms of natural and man-made materials (Gadd, 1993, 1999; Burford et al., 2003a). A fungal role in biogeochemical cycling of the elements (e.g. C, N, P, S, metals) is obvious and interlinked with the ability to adopt a variety of growth, metabolic and morphological strategies, their adaptive capabilities to environmental extremes and their symbiotic associations with animals, plants, algae and cyanobacteria (Burford et al., 2003a; Braissant et al., 2004; Gadd, 2004). Fungal polymorphism and reproduction by spores underpin successful colonization of different environments. Most fungi exhibit a filamentous growth habit, which provides an ability for adoption of either explorative or exploitative growth strategies, and the formation of linear organs of aggregated hyphae for protected fungal translocation (see Fomina et al., 2005b). Some fungi are polymorphic, occurring as both filamentous mycelium and unicellular yeasts or yeast-like cells, e.g. black meristematic or microcolonial fungi colonizing rocks (Sterflinger, 2000; Gorbushina et al., 2002, 2003). Fungi can also grow inside their own parental hyphae utilizing dead parts of the colony under the protection of parental cell walls (Gorbushina et al., 2003). The ability of fungi to translocate nutrients through the mycelial network is another important feature for exploring heterogeneous environments (Jacobs et al., 2002, 2004; Lindahl & Olsson, 2004).

The earliest fossil record of fungi in terrestrial ecosystems occurred during the Ordovician period (480 to 460 MYBP) (Heckman et al., 2001).

Introduction

The mycelium of woodland fungi can act both as a reservoir and as a distribution system for nutrients, owing to its physiological and developmental adaptations to life at the interface between organic and mineral soil horizons. The mobility of accumulated nitrogen and phosphorus within the mycelial networks of cord-forming wood decay fungi and ectomycorrhiza enables fungi to play key roles as wood decomposers and root symbionts. The dynamics of nitrogen movement have been less investigated than phosphorus owing to lack of a suitable tracer. We have developed a new technique for tracing nitrogen translocation in real time, using 14C as a marker for nitrogen by incorporating it into a non-decomposed amino acid that tracks the mycelial free amino acid pool. Its movement can be imaged by counting photon emissions from a scintillant screen in contact with the mycelial system. This method allows real-time imaging at high temporal and spatial resolution, for periods of weeks and areas up to 1 m2, in microcosms that mimic the mineral/organic soil interface of the forest floor. The results reveal a hitherto unsuspected dynamism and responsiveness in amino acid flows through mycelial networks of cord-forming, wood-decomposing basidiomycetes. We interpret these in the light of current understanding of the pivotal role of fungi in boreal and temperate forest floor nutrient cycling, and attempt to formulate key questions to investigate the effects of mycelial nitrogen translocation on forest floor decomposition and nitrogen absorption.

Introduction

Oceans cover around 70% of the global surface area, yet remain one of the least explored regions for fungal diversity; consequently knowledge of the fungal contribution to ecosystem processes in these marine environments is extremely limited. For the purposes of this review, marine habitats are defined as those influenced in some way by seawater, generally from existing saline water bodies. In some cases, saline habitats have resulted from salt accumulation in soils originating from ancient seas. Broadly, marine ecosystems divide between those influenced in some way by terrestrial environments, generally situated close to coastal regions, and those associated with the open ocean. Broad boundaries within marine environments are detailed in Table 18.1, where coastal and open ocean, and the effect of depth within open oceans, is differentiated. Marine environments tend also to be strongly linked, representing movement between different regions of seas and oceans, as summarized in Fig. 18.1. In coastal regions, numerous types of marine environment develop, including saline wetlands and lagoons on low-energy coasts, estuarine systems where there is freshwater influx, and a range of beach and splash communities on high-energy coasts. Such ecosystems are reviewed in more detail by Packham and Willis (1997). Adjacent to coastal regions, and where continental shelves are shallow, coastal sea communities form, including coral reefs, which are found in both tropical and cold seas. A number of inland saline environments also exist, such as salt pans and salt deserts.