Fundamentals of microbial community resistance and resilience

Fundamentals of microbial community resistance and resilience

December 2012 | Ashley Shade, Hannes Peter, Steven D. Allison, Didier L. Baho, Mercè Berga, Helmut Bürgmann, David H. Huber, Silke Langenheder, Jay T. Lennon, Jennifer B. H. Martiny, Kristin L. Matulich, Thomas M. Schmidt, Jo Handelsman
Microbial communities are central to all ecosystems, yet their responses to disturbances remain challenging to measure and predict. Understanding factors that drive microbial community stability, including resistance (insensitivity to disturbance) and resilience (rate of recovery after disturbance), is crucial for predicting community responses to disturbances. This review provides an overview of key concepts related to microbial community stability, including insights from ecology, studies on community responses to pulse and press disturbances, and biological features that influence stability. It also discusses how systems-level perspectives, informed by meta-omics data, can enhance understanding of microbial community stability. Disturbances are events that alter the environment or directly affect communities. They can be classified as pulses (short-term) or presses (long-term). Stability is defined as a community's response to disturbance, encompassing resistance (insensitivity to disturbance) and resilience (rate of recovery). Resistance is the degree to which a community is insensitive to a disturbance, while resilience is the rate at which a community returns to a pre-disturbance condition. These metrics are useful for comparing community disturbance responses and have precedent in microbial ecology. Microbial communities may exhibit different responses to pulse and press disturbances. Pulse disturbances are short-term events, while press disturbances are long-term or continuous. The distinction between pulse and press disturbances is important for understanding microbial community responses, especially in the context of global climate change, where pulse disturbances (e.g., extreme weather events) are expected to increase in frequency, and ongoing press disturbances (e.g., atmospheric increases in carbon dioxide, ocean acidification) are expected to continue. Microbial community stability can be investigated through functional or compositional parameters. Functional and compositional stability may be related, depending on the function of interest. For functions carried out by many taxa, changes in community composition may not correspond with changes in functional rates. For functions performed by only a few taxa, sensitivity and resilience may closely follow changes in the abundance of those taxa. Studies of alternative stable states and regime shifts in microbial systems are rare, though the conceptual framework is gaining popularity, especially among researchers interested in the human gut microbiome. There is also evidence of alternative stable states in the vaginal microbiome, where eight "super-groups" of distinct microbial assemblages have been detected across hundreds of healthy women. Additionally, there are a few concrete examples of microbial communities that exhibited regime shifts. Measuring stability involves distinguishing between responses to pulse and press disturbances, as recovery may be quantified by slightly different methods. Community resilience is represented by the slope of the basin walls, showing a rate of return to the original stable state. Experimental settings allow pulse and press responses to be compared directly and described relative to one another. Community invasibility can provide an indicator for both compositional and functional stability. Invasion is unique in that it can be considered both a cause and consequence of disturbance. In studies of communities with larger organisms, a well-known consequence of community disturbance is reduced resistance to invasion by alien species (called "nicMicrobial communities are central to all ecosystems, yet their responses to disturbances remain challenging to measure and predict. Understanding factors that drive microbial community stability, including resistance (insensitivity to disturbance) and resilience (rate of recovery after disturbance), is crucial for predicting community responses to disturbances. This review provides an overview of key concepts related to microbial community stability, including insights from ecology, studies on community responses to pulse and press disturbances, and biological features that influence stability. It also discusses how systems-level perspectives, informed by meta-omics data, can enhance understanding of microbial community stability. Disturbances are events that alter the environment or directly affect communities. They can be classified as pulses (short-term) or presses (long-term). Stability is defined as a community's response to disturbance, encompassing resistance (insensitivity to disturbance) and resilience (rate of recovery). Resistance is the degree to which a community is insensitive to a disturbance, while resilience is the rate at which a community returns to a pre-disturbance condition. These metrics are useful for comparing community disturbance responses and have precedent in microbial ecology. Microbial communities may exhibit different responses to pulse and press disturbances. Pulse disturbances are short-term events, while press disturbances are long-term or continuous. The distinction between pulse and press disturbances is important for understanding microbial community responses, especially in the context of global climate change, where pulse disturbances (e.g., extreme weather events) are expected to increase in frequency, and ongoing press disturbances (e.g., atmospheric increases in carbon dioxide, ocean acidification) are expected to continue. Microbial community stability can be investigated through functional or compositional parameters. Functional and compositional stability may be related, depending on the function of interest. For functions carried out by many taxa, changes in community composition may not correspond with changes in functional rates. For functions performed by only a few taxa, sensitivity and resilience may closely follow changes in the abundance of those taxa. Studies of alternative stable states and regime shifts in microbial systems are rare, though the conceptual framework is gaining popularity, especially among researchers interested in the human gut microbiome. There is also evidence of alternative stable states in the vaginal microbiome, where eight "super-groups" of distinct microbial assemblages have been detected across hundreds of healthy women. Additionally, there are a few concrete examples of microbial communities that exhibited regime shifts. Measuring stability involves distinguishing between responses to pulse and press disturbances, as recovery may be quantified by slightly different methods. Community resilience is represented by the slope of the basin walls, showing a rate of return to the original stable state. Experimental settings allow pulse and press responses to be compared directly and described relative to one another. Community invasibility can provide an indicator for both compositional and functional stability. Invasion is unique in that it can be considered both a cause and consequence of disturbance. In studies of communities with larger organisms, a well-known consequence of community disturbance is reduced resistance to invasion by alien species (called "nic
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