Role Of Microbial Communities In Mediating Ecosystem Response To Disturbance

Research on decomposer communities of terrestrial ecosystems for a long time has focussed on microbial biomass and gross turnover parameters. Recently, more and more attempts are made to look beyond the biomass, and more specifically determine functions and populations on a smaller scale-in time and space. A multitude of techniques is being improved and developed. Garland and Mills (1991) triggered a series of publications on substrate utilization tests in the field of microbial ecology. Despite several promising results for different applications in different laboratories, many problems concerning the assay and the interpretation of results became evident. After individual discussions on the approach with colleagues from various laboratories we started to plan a workshop on the matter. The response on our first circular was extraordinary, and instead of a small workshop it became a meeting with almost 150 participants. The meeting was named 'Substrate use for characterization of microbial communities in terrestrial ecosystems' (SUBMECO) and was held in Innsbruck, Austria, from Oct. 16-18, 1996. The very focussed scope attracted enthusiastic advocates of the approach, and also serious critics. Some of the topics concerned improvements of current inoculation and incubation techniques, ranging from sample pre-treatment, inoculum density and incubation temperature to statistical data handling. New methods for calculating microbial diversity were proposed, as well as bootstrap methods that allow statistics with many variables on a relatively low number of replicates.

Tropical ecosystems are different in important ways from those of temperate regions. They are a major reservoir of plant and animal biodiversity and play important roles in global climate regulation and biogeochemical cycling. They are also under great threat due to the conversion of tropical ecosystems to other uses. Thus, in the context of global change, it is crucial to understand how environmental factors, biogeographic patterns, and land use changes interact to influence the structure and function of microbial communities in these ecosystems. The contributions to this Research Topic showcase the current knowledge regarding microbial ecology in tropical ecosystems, identify many challenges and questions that remain to be addressed and open up new horizons in our understanding of the environmental and anthropological factors controlling microbial communities in these important ecosystems.

Understanding the link between microbial diversity and ecosystem processes is a fundamental goal of microbial ecologists, yet we still have a rudimentary knowledge of how changes in diversity affect nutrient cycling and energy transfer in ecosystems. Due to the complexity of the problem, many published studies on this topic have been conducted in artificial or manipulated systems. Although researchers have begun to expose some possible mechanisms using these approaches, most have not yet been able to produce conclusive results that relate directly to natural systems. The few studies that have explored the link between diversity and activity in natural systems have typically focused on specific nutrient cycles or processes, such as nitrification, denitrification, and organic carbon degradation pathways, and the microbes that mediate them. What we have learned from these studies is that there are often strong associations between the physical and chemical features of the environment, the composition of the microbial communities, and their activities, but the rules that govern these associations have not been fully elucidated. These earlier studies of microbial diversity and processes in natural systems provide a framework for additional studies to broaden our understanding of the role of microbial diversity in ecosystem function. The problem is complex, but with recent advances in sequencing technology, -omics, and in-situ measurements of ecosystem processes and their applications to microbial communities, making direct connections between ecosystem function and microbial diversity seems more tractable than ever.

Beginning with the germ theory of disease in the 19th century and extending through most of the 20th century, microbes were believed to live their lives as solitary, unicellular, disease-causing organisms . This perception stemmed from the focus of most investigators on organisms that could be grown in the laboratory as cellular monocultures, often dispersed in liquid, and under ambient conditions of temperature, lighting, and humidity. Most such inquiries were designed to identify microbial pathogens by satisfying Koch's postulates.3 This pathogen-centric approach to the study of microorganisms produced a metaphorical "war" against these microbial invaders waged with antibiotic therapies, while simultaneously obscuring the dynamic relationships that exist among and between host organisms and their associated microorganisms-only a tiny fraction of which act as pathogens. Despite their obvious importance, very little is actually known about the processes and factors that influence the assembly, function, and stability of microbial communities. Gaining this knowledge will require a seismic shift away from the study of individual microbes in isolation to inquiries into the nature of diverse and often complex microbial communities, the forces that shape them, and their relationships with other communities and organisms, including their multicellular hosts. On March 6 and 7, 2012, the Institute of Medicine's (IOM's) Forum on Microbial Threats hosted a public workshop to explore the emerging science of the "social biology" of microbial communities. Workshop presentations and discussions embraced a wide spectrum of topics, experimental systems, and theoretical perspectives representative of the current, multifaceted exploration of the microbial frontier. Participants discussed ecological, evolutionary, and genetic factors contributing to the assembly, function, and stability of microbial communities; how microbial communities adapt and respond to environmental stimuli; theoretical and experimental approaches to advance this nascent field; and potential applications of knowledge gained from the study of microbial communities for the improvement of human, animal, plant, and ecosystem health and toward a deeper understanding of microbial diversity and evolution. The Social Biology of Microbial Communities: Workshop Summary further explains the happenings of the workshop.

A central goal of global change biology is to predict the impact of environmental change on ecosystem processes. Currently, most global change models treat the local microbial community as a single, homogenously functioning entity, thereby assuming that the specific microbial composition is functionally irrelevant. However, microorganisms perform key transformations in ecosystems, and recent research demonstrates that microbial communities vary greatly across space and in response to environmental change. Therefore, parameters describing microbial communities may be key for improving predictions of how future global changes will impact ecosystem processes. For this reason, my dissertation research examined the effect of environmental changes on resident communities and determined how potential shifts in microbial community composition will impact litter decomposition rates. To accomplish this, I gathered litter samples from a chaparral ecosystem undergoing global change manipulations (elevated nitrogen availability or reduced precipitation), and characterized the microbial community using 454 high-throughput sequencing (Chapter 1). While microbial communities are much more variable through time, this research showed that microbial composition will likely shift in response to environmental change. I also examined the role of microbial community composition for a key ecosystem process, litter decomposition, and how that role changes under environmental perturbations. By isolating microbial taxa from the same ecosystem discussed above, I constructed artificial microbial communities with varying composition. I then conducted a laboratory experiment in which I subjected the communities to different global change manipulations and monitored decomposition rates and community composition (Chapter 2). Microbial composition had a main effect on leaf litter decomposition and also interacted with the environmental treatment, suggesting that future shifts in microbial communities will influence the magnitude in which environmental change affects ecosystem processes. Lastly, I investigated the functional and response traits of individual microbial taxa to better predict how microbial communities might respond to global change perturbations, and found that many functional traits displayed a phylogenetic pattern, but a taxa's response to increased temperature did not (Chapter 3). Ultimately, this set of studies further justifies the need to incorporate microbial communities into models and begins to identify which parameters might be most relevant.

The cryosphere stands for environments where water appears in a frozen form. It includes permafrost, glaciers, ice sheets, and sea ice and is currently more affected by Global Change than most other regions of the Earth. In the cryosphere, limited water availability and subzero temperatures cause extreme conditions for all kind of life which microorganisms can cope with extremely well. The cryosphere’s microbiota displays an unexpectedly large genetic potential, and taxonomic as well as functional diversity which, however, we still only begin to map. Also, microbial communities influence reaction patterns of the cryosphere towards Global Change. Altered patterns of seasonal temperature fluctuations and precipitation are expected in the Arctic and will affect the microbial turnover of soil organic matter (SOM). Activation of nutrients by thawing and increased active layer thickness as well as erosion renders nutrient stocks accessible to microbial activities. Also, glacier melt and retreat stimulate microbial life in turn influencing albedo and surface temperatures. In this context, the functional resilience of microbial communities in the cryosphere is of major interest. Particularly important is the ability of microorganisms and microbial communities to respond to changes in their surroundings by intracellular regulation and population shifts within functional niches, respectively. Research on microbial life exposed to permanent freeze or seasonal freeze-thaw cycles has led to astonishing findings about microbial versatility, adaptation, and diversity. Microorganisms thrive in cold habitats and new sequencing techniques have produced large amounts of genomic, metagenomic, and metatranscriptomic data that allow insights into the fascinating microbial ecology and physiology at low and subzero temperatures. Moreover, some of the frozen ecosystems such as permafrost constitute major global carbon and nitrogen storages, but can also act as sources of the greenhouse gases methane and nitrous oxide. In this book we summarize state of the art knowledge on whether environmental changes are met by a flexible microbial community retaining its function, or if the altered conditions also render the community in a state of altered properties that affect the Earth’s element cycles and climate. This book brings together research on the cryosphere’s microbiota including permafrost, glaciers, and sea ice in Arctic and Antarctic regions. Different spatial scales and levels of complexity are considered, spanning from ecosystem level to pure culture studies of model microbes in the laboratory. It aims to attract a wide range of parties with interest in the effect of climate change and/or low temperatures on microbial nutrient cycling and physiology.

Recent developments in various “OMICs” fields have revolutionized our understanding of the vast diversity and ubiquity of microbes in the biosphere. However, most of the current paradigms of microbial cell biology, and our view of how microbes live and what they are capable of, are derived from in vitro experiments on isolated strains. Even the co-culturing of mixed species to interrogate community behavior is relatively new. But the majority of microorganisms lives in complex communities in natural environments, under varying conditions, and often cannot be cultivated. Unless we obtain a detailed understanding of the near-native 3D ultrastructure of individual community members, the 3D spatial community organization, their metabolic interdependences, coordinated gene expression and the spatial organization of their macromolecular machines inventories as well as their communication strategies, we won’t be able to truly understand microbial community life. How spatial and also temporal organization in cell–cell interactions are achieved remains largely elusive. For example, a key question in microbial ecology is what mechanisms microbes employ to respond when faced with prey, competitors or predators, and changes in external factors. Specifically, to what degree do bacterial cells in biofilms act individually or with coordinated responses? What are the spatial extent and coherence of coordinated responses? In addition, networks linking organisms across a dynamic range of physical constraints and connections should provide the basis for linked evolutionary changes under pressure from a changing environment. Therefore, we need to investigate microbial responses to altered or adverse environmental conditions (including phages, predators, and competitors) and their macromolecular, metabolic responses according to their spatial organization. We envision a diverse set of tools, including optical, spectroscopical, chemical and ultrastructural imaging techniques that will be utilized to address questions regarding e.g. intra- and inter-organism interactions linked to ultrastructure, and correlated adaptive responses in gene expression, physiological and metabolic states as a consequence of the alterations of their environment. Clearly strategies for co-evolution and in general the display of adaptive strategies of a microbial network as a response to the altered environment are of high interest. While a special focus will be placed on terrestrial sole-species or mixed biofilms, we are also interested in aquatic systems, biofilms in general and microbes living in symbiosis. In this Research Topic, we wish to summarize and review results investigating interactions and possibly networks between microbes of the same or different species, their co-occurrence, as well as spatiotemporal patterns of distribution. Our goal is to include a broad spectrum of experimental and theoretical contributions, from research and review articles to hypothesis and theory, aiming at understanding microbial interactions at a systems level.