FUNGI IN ECOSYSTEM PROCESSES - CHAPTER 1 potx

Fungi Pathogenic for Humans and Animals in three parts, edited by Dexter H Howard 4 Fungal Differentiation A Contemporary Synthesis, edited by John E.. Smith 5 Secondary Metabolism and D

Fungi in Ecosystem Processes

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MYCOLOGY SERIES

Editor

J W Bennett

ProfessorDepartment of Cell and Molecular Biology

Tulane UniversityNew Orleans, Louisiana

Founding Editor

Paul A Lemke

1 Viruses and Plasmids in Fungi, edited by Paul A Lemke

2 The Fungal Community Its Organization and Role in the

Ecosys-tem, edited by Donald T Wicklow and George C Carroll

3 Fungi Pathogenic for Humans and Animals (in three parts), edited

by Dexter H Howard

4 Fungal Differentiation A Contemporary Synthesis, edited by John

E Smith

5 Secondary Metabolism and Differentiation in Fungi, edited by Joan

W Bennett and Alex Ciegler

6 Fungal Protoplasts, edited by John F Peberdy and Lajos Ferenczy

7 Viruses of Fungi and Simple Eukaryotes, edited by Yigal Koltm and

Michael J Leibowitz

8 Molecular Industrial Mycology: Systems and Applications for

Fila-mentous Fungi, edited by Sally A Leong and Randy M Berka

9 The Fungal Community Its Organization and Role in the

Eco-system, Second Edition, edited by George C Carroll and Donald T

Wicklow

10 Stress Tolerance of Fungi, edited by D H Jennings

11 Metal Ions in Fungi, edited by Gunther Wmkelmann and Dennis R

Wmge

12 Anaerobic Fungi Biology, Ecology, and Function, edited by

Douglas O Mountfort and Colin G Orpin

13 Fungal Genetics Principles and Practice, edited by Cees J Bos

14 Fungal Pathogenesis Principles and Clinical Applications, edited

by Richard A Calderone and Ronald L Cihlar

15 Molecular Biology of Fungal Development, edited by Heinz D

Osie-wacz

16 Pathogenic Fungi in Humans and Animals: Second Edition, edited

by Dexter H Howard

17 Fungi in Ecosystem Processes, John Dighton

18 Genomics of Plants and Fungi, edited by Rolf A Prade and Hans J.

Bohnert

Additional Volumes in Preparation

Clavicipitalean Fungi: Evolutionary Biology, Chemistry, Biocontrol, and Cultural Impacts, edited by James F White, Jr, Charles W.

Bacon, Nigel L Hywel-Jones, and Joseph W Spatafora

Why did I decide to write this book? As an undergraduate student I could notmake up my mind whether I wanted to be a zoologist or a botanist, so I decided toadopt ecology, in its broadest sense, as my area of interest This led me to thinkabout interactions among organisms and to try to look at ecosystems from aholistic, rather than from an autecological, point of view As someone with littleformal training in mycology, my interest in fungi started during my doctoralresearch, especially when attending university-wide lectures by C T Ingold,given at the University of London My former job, at the then Institute ofTerrestrial Ecology at Merlewood, UK, brought me into contact with the work onectomycorrhizae, decomposition, and nutrient cycling in temperate andsubtropical forest ecosystems During this time, I had many fruitful discussionswith fungal ecologists in both the British Mycological Society and theinternational world of mycorrhizal researchers In particular, I rememberanimated discussions with Alan Rayner, who is a font of knowledge, inspiration,and encouragement As a result of this history, I have been fascinated by themultifarious ways in which fungi interact with other organisms and function inmoderating the processes occurring in ecosystems

With my move to Rutgers University, I initially taught my first graduatecourse, Fungi in Ecosystems, during my first semester, while all my books andnotes were on a ship crossing the Atlantic The continued development of thiscourse has been the impetus for this book As I could find no textbook for mystudents that really approached the subject of mycology from an ecosystem point

of view, I decided to put my ideas on the importance of fungi in ecosystemprocesses into a volume that could be used by upper-level students and

researchers This course and its variants have been the main thrust of my teaching

at Rutgers This has not been a sole venture as, along with my interactions withJim White and Peter Oudemans, we are gradually building a strong andinteractive series of mycology courses in our university

In this book I have started with the list of functions that Alan Raynersuggests that fungi perform in ecosystems (introduction to the second edition ofThe Fungal Community: Its Structure and Function, edited by George C Carrolland Donald T Wicklow, (Marcel Dekker, 1992)) I have attempted to elaborate

on these functional roles of fungi and tried to show how the world would functionless satisfactorily in the absence of fungi Given the vast range of fungal literature

I have not been able to do much more than scratch the surface of the subject.However, I hope that the more than 1300 references that I have cited will act as ameans for interested readers to delve further into the literature on any specificsubject area For the upper-level students and researchers to whom this book istargeted, I hope that it will stimulate thoughts beyond the narrow confines of theirimmediate research questions and allow them to place their work in the widercontext of the functioning of ecosystems I believe that it is only by the greaterunderstanding of the linkages between organisms and the processes they control

in the ecosystem that we can appreciate the beauty of the living world around us,appreciate the impacts that we are having on ecosystems, and obtain theunderstanding of the function of component organisms that will allow us toprotect and preserve nature

In attempting to summarize the vast literature, I have written the text in myown words, but have relied heavily on previously published literature for figuresand tables to support my commentary Most tables have been reconstructed andalmost all figures have been redrawn from their original in an effort to simplifythe information presented in the originals For the statistical purist, I hope that myremoval of error bars and indications of significant differences will be forgivenfor the sake of simplicity of presentation In the main, the data shown in figuresrepresent statistically significant interactions Although the figures and tablesrepresent the key message I wish to convey, they are no substitute for the originaldata and publications I encourage the interested reader to explore further byconsulting the original publications to obtain more information that I can impart

in this book

I dedicate this book to my uncle, Wally Champkin, whose enthusiasm fornatural history fueled my interest in ecology As a child I was constantly amazedthat he could put a name to most of the plants, insects, and birds we saw on ourwalks I could watch for hours his cine films and stills of birds, flowers, moths,and butterflies I owe a debt of gratitude to my parents, who encouraged andsupported me in my studies and allowed me to pursue my own interests inbiology I especially thank my wife, Joan, and daughter, Gail, who havesupported my career, moved with me to the United States, and encouraged me in

Prefaceiv

the writing of this book I could not have completed this task without them.Finally, I wish to thank Bob Evans, who commented on the first drafts of my workhere, and to the students and colleagues in my research group, who have bothgiven me encouragement and tolerated my absences during the creation of thisbook.

John Dighton

Preface

1 Introduction1.1 Why Fungi?

1.2 What Are Ecosystems and Ecosystem Functions?

1.3 What Are Fungi?

1.4 Specific Ecosystem Services Carried Out by Fungi1.5 Concluding Remarks

3.4 Interactions Among Mycorrhizae and Plant Pathogens3.5 Synopsis and Outlook

4.5 Fungal – Faunal Interactions in Aquatic and MarineEcosystems

4.6 Summary and ConclusionsReferences

5 Fungi and Population and Community Regulation5.1 Mycorrhizae and Plant Successions

5.2 Mycorrhizae and Plant Fitness5.3 Plant Pathogens and Plant Fitness5.4 Saprotroph – Pathogen Interactions: Biocontrol5.5 Mycorrhizae – Pathogen Interactions

5.6 Endophytes and Antiherbivore Action5.7 Nematophagous Fungi and Animal Pathogens5.8 Allelopathy

5.9 Summary and DiscussionReferences

6 Fungal Interactions with Humans6.1 Introduction

6.2 Fungi and Acidifying Pollutants6.3 Fungi and Heavy Metals6.4 Fungi and Radionuclides6.5 Fungi and Climate Change6.6 Concluding RemarksReferences

7 Synopsis and Outlook to the Future7.1 Introduction

7.2 The Ecosystem

Contentsviii

7.3 The Fungal Organism7.4 The Fungal Community7.5 Perturbations

7.6 Fungi in Ecosystems: What Next?

References

1 Introduction

1.1 WHY FUNGI?

The first law of thermodynamics indicates that matter can neither be created nordestroyed Within ecosystems, this law governs the transformations of energyand nutrients between compartments Energy and nutrients are contained withinthe living biomass of the plants and animals forming communities within theecosystem as energy and nutrient stores The transformations of energy andnutrients that occur among these is a result of trophic interactions within foodchains and webs and are regarded as the processes that occur in ecosystems Thenature of these stores of nutrients and energy within individual organisms andcommunities and the movement of material among them is the science ofecology We will consider here the role that fungi play in some of the majorecosystem processes, namely the process of transforming carbon dioxide andnutrients into plant biomass by photosynthesis, the energy and nutrienttransformations among components of food webs, and the transformationscarried out by saprotrophic decomposers that use the energy and nutrients fromdead plants and animals, resulting in the mineralization of nutrients for new plantgrowth This latter process is referred to as energy and nutrient cycling Inaddition, we will explore the interactions of human influence on the processescarried out by fungi in the ecosystem

Fungi are a group of organisms that cannot fix energy directly, but they usethe energy stored in plant and animal biomass to create their own mass It is thevast array of interactions among fungi, and other living and dead organisms alongwith their interaction with the nonliving components of the environment thatmake fungi a key group of organisms in the regulation of ecosystem processes.Fungi are important in driving or controlling the mineral and energy cyclingwithin ecosystems and influencing the composition of other organisms within theecosystem

needed to build cytoplasm and structural components of plant biomass Some ofthese nutrients come directly from mineral soil; however, much is recycled withinthe ecosystem Nutrients that are locked up in plant and animal biomass becomeavailable to the saprotrophic community upon the death of the organism Thesaprotrophic community, consisting largely of fungi and bacteria, utilizes theenergy and nutrients contained in the dead material, but through “leakiness” of itsactivities, allows a proportion of the nutrients to become available to otherorganisms through the process of nutrient mineralization This leakiness is aresult of the inefficiencies in utilizating the end products of the activity ofextracellular enzyme activity The absorption of reaction products is never 100%efficient, and the mineralized nutrients that are not absorbed by the fungus arereleased into the environment and are accessible by other organisms Forexample, this activity provides soil fertility for plant growth or increased nutrientcontent of streams for the growth of algae We will discuss the role of fungi inboth the direct support of photosynthetic activities, mainly within lichens, and incontrolling the availability of mineral nutrients in the environment that can beused by autotrophs Within this context we will discuss the role of lichen,saprotrophic, and mycorrhizal fungi.

The organisms that make up the biotic component of ecosystems coexist incommunities The interactions among members of the community can involvecompetition for available resources (e.g., food, light, and space) or competitionamong trophic levels in producer – consumer and predator – prey food webinteractions (For a review of communities, see Morin, 1999.) Within the context

of population regulation of plants or animals, fungi play an important role aspathogens Subtle interactions among fungi and plants and animals may alterthe fitness of individuals or species within the community without showing theoutward signs of pathogenicity Fungal interaction with plants can be seen in theform of pathogens, which are detrimental to plant growth and fitness:mycorrhizae, which help plants obtain nutrients and provide defense againstpathogens, and endophytes, which provide defense against herbivory andimprove nutrient levels in the plant In addition, fungi themselves play animportant and direct role within food webs in ecosystems by being consumed byfungal grazers, and as dead organisms, by the saprotrophic activities of bacteriaand other fungi within the ecosystem Fungi are thus important in determining thepopulation of individuals of a species in a community and the speciescomposition or structure of that community

The increasingly important role of humans on the landscape in mostecosystems around the world adds another dimension to the role of fungi in theenvironment Because of the relatively short generation times of microbes,particularly bacteria, fungi and actinomycetes are able to more rapidly evolveresistance to disturbance than other “higher” organisms The effects of humaninteractions in the environment can thus have a detrimental effect on

the communities of fungi as well as their physiology and biochemistry Fungi arealso able to adapt to new conditions and have the capacity to utilize pollutantsproduced by anthropogenic activities, however The role of fungi in heavy metaland radionuclide-polluted environments will be used as examples of the potentialrole of fungi in remediation of polluted ecosystems and other biogeochemicalprocesses.

1.3 WHAT ARE FUNGI?

We will not dwell on the taxonomy and structure of fungi, as these topics areadequately discussed in other texts (Alexopoulus and Mims, 1979; Moore-Landecker, 1996; Kendrick, 1992; Hawksworth et al., 1995) We will, however,review some of the key features of the fungal body and its physiology that allowfungi to make an important contribution to ecosystem processes The taxonomy

of fungi is constantly in debate and there are continual changes in terms of thecategory under which species should be organized and in terms of thenomenclature of each of the hierarchical categories For the purposes of ourdiscussion of the role of fungi in ecosystem functions, we can say that all taxa offungi may be involved in the processes that are described (with certainrestrictions), but the details of involvement may depend upon taxonomic statusand life history traits Of these traits we will mention the general models of r-, K-and R – C – S selection strategies, as defined by Pianka (1970) and Grime (1977;1979), respectively (Fig 1.1) The application of these strategies has beendiscussed in relation to the ecology of saprotrophic fungi (Cooke and Rayner,1984) and mycorrhizal fungi (Dighton et al., 1986; Allen, 1991) The r – Kcontinuum contends that organisms lie along a gradient of extremes in whichr-selected organisms are opportunistic, are combatitive by virtue of fast growth,have a high turnover rate, have low investment in biomass and functionalattributes (e.g., enzymatic diversity), and produce many offspring, many of whichwill not survive The K strategist has the opposite traits of longevity, investmentinto biomass, and functional attributes, is combatitive by virtue of development

of defense mechanisms, and produces few offspring, each with a greater chance

of survival

The R – C – S selection strategy is possibly a more useful theoretic concept

in which to discuss the behavior of fungi In this system, the extreme positionscan be considered as the apices of a triangle R-selected organisms are ruderals,having similar survival strategies of r-selected organisms They are quick tocolonize new resources, invest little energy and resources in biomass orenzymatic function, and are outcompeted by fungal species that are more able toproduce secondary metabolites for defense The C strategists are combatitiveand are equivalent to the K strategists of Pianka (1970) C strategists are slow-growing but invest resources in biomass and such functional processes as

Chapter 18

production of enzymes and secondary metabolites for defense The third apex ofthe triangle is the S, or stress-tolerant, strategist These exist because they areable to withstand a sustained stress within the environment (e.g., temperature,salinity, heavy metals) They resemble the C strategists in their physiologicaland life history traits It is their ability to produce secondary metabolites orbuild defensive mechanisms in their biomass that enables them to withstand thesustained environmental stress under which they live Upon removal of thestress, the S strategists will be less competitive against C strategists, resulting in

a change in the community structure of the fungal populations As resources inthe environment become available for fungal colonization (e.g., new leaf litterduring the fall) successions of fungi colonizing the resource tend to follow atrajectory from r (or R) strategists to K (or C) strategists (Andrews, 1992;Frankland, 1992) Both life history strategy simplify reality, but allow us toidentify similarities and differences between fungal ecophysiology and changes

in the environmental conditions in which they live More complicated, but morerealistic, models have been developed (Andrews, 1992) These simplistic

FIGURE1.1 Life history strategies as applied to fungi, contrasting the r – K concept ofPianka (1970) with the R – C – S strategy of Grime (1977; 1979)

models, however, serve a useful context in which to understand the changes infungal communities during the utilization of resources and in the face ofdisturbance.

A stylized fungal organism is shown in Fig 1.2, along with some of theproperties that make it important in the context of this discussion The mycelialportion of the fungus consists of hyphae These hyphae, which are absent in theChytridomycetes and yeasts, are a filamentous assemblage of tubular cells inwhich continuity is maintained between adjacent cells by the absence of cross-cell walls (septa) or a septum perforated by a pore The hyphae thus develop as

a coenocytic structure, consisting of continual cytoplasmic connectivitybetween adjacent cells Hyphae average 5 – 6 mm in diameter and grow bywall extension at the tip (Rayner, 1991) Because they have a narrow diameterand long length, fungal hyphae present a large surface area, relative to volume,

to the environment around them (Table 1.2) This property allows fungi tooptimize the absorption of degradation products of simple carbohydrates andmineral nutrients that are derived from the action of extracellular enzymesproduced by the fungi Fungal hyphae may grow independently or coalesce toform larger and structured assemblages called rhizomorphs or strands These

FIGURE1.2 Diagrammatic representation of a fungus showing the branching of hyphaewithin the mycelium, aggregation of hyphae into cords, and the development of fruitingstructures for spore dissemination

Chapter 110