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1. Exploring Microbiome Functional Dynamics through Space and Time with Trait-Based Theory

   https://doi.org/10.1128/mSystems.00530-21  

   Bittleston, Leonora S. ; Freedman, Zachary B. ; Bernardin, Jessica R. ; Grothjan, Jacob J. ; Young, Erica B. ; Record, Sydne ; Baiser, Benjamin ; Gray, Sarah M. ; Malik, Ashish ( August 2021 , mSystems)

   Shade, Ashley (Ed.)

   ABSTRACT Microbiomes play essential roles in the health and function of animal and plant hosts and drive nutrient cycling across ecosystems. Integrating novel trait-based approaches with ecological theory can facilitate the prediction of microbial functional traits important for ecosystem functioning and health. In particular, the yield-acquisition-stress (Y-A-S) framework considers dominant microbial life history strategies across gradients of resource availability and stress. However, microbiomes are dynamic, and spatial and temporal shifts in taxonomic and trait composition can affect ecosystem functions. We posit that extending the Y-A-S framework to microbiomes during succession and across biogeographic gradients can lead to generalizable rules for how microbiomes and their functions respond to resources and stress across space, time, and diverse ecosystems. We demonstrate the potential of this framework by applying it to the microbiomes hosted by the carnivorous pitcher plant Sarracenia purpurea , which have clear successional trajectories and are distributed across a broad climatic gradient. 

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2. Drought legacies mediated by trait trade‐offs in soil microbiomes

   https://doi.org/10.1002/ecs2.3562  

   Wang, Bin ; Allison, Steven D. ( June 2021 , Ecosphere)

   Soil microbiomes play a key role in driving biogeochemical cycles of the Earth system. As drought frequency and intensity increase due to climate change, soil microbes and the processes they control will be impacted. Even after a drought ends, microbiomes and other systems take time to recover and may display a memory of previous climate conditions. Still, the mechanisms involved in these legacy effects remain unclear, making it difficult to predict climate and biogeochemical rates in the future. Here, we used a trait‐based microbiome model (DEMENTpy) to implement trade‐off‐mediated mechanisms that may lead to drought legacy effects on litter decomposition. Trade‐offs were assumed to follow the Y‐A‐S framework that defines three primary life‐history strategies of microorganisms: high growth Yield, resource Acquisition, and Stress tolerance. We represented cellular trade‐offs between osmolytes required for drought tolerance and investment in enzymes involved in litter decomposition. Simulations were run under varying levels of drought severity and dispersal. With high levels of dispersal, no legacy effects were predicted by DEMENTpy following drought. With limited dispersal, severe drought resulted in a persistent legacy of altered community‐level traits and reduced litter decomposition. Moderate drought resulted in a transient legacy that disappeared after two years, consistent with recent empirical observations in Southern California ecosystems. These results imply that greater movement along the trade‐off between enzyme investment and osmolyte production resulted in stronger legacy effects. More generally, factors that shift the position of a microbiome in YAS space may alter the legacy outcome following drought. Our trait‐based modeling study motivates additional empirical measurements to quantify YAS traits and trade‐offs that are needed to make accurate predictions of soil microbiome resilience and functioning. Also, our study illustrates an emerging approach for representing trait trade‐offs in microbiomes and vegetation that dictate ecosystem responses to drought and other environmental perturbations.

    

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3. Drought response in herbaceous plants: A test of the integrated framework of plant form and function

   https://doi.org/10.1111/1365-2435.14495  

   Funk, Jennifer L. ; Larson, Julie E. ; Blair, Megan D. ; Nguyen, Monica A. ; Rivera, Ben J. ( January 2024 , Functional Ecology)

   Multidimensional trait frameworks are increasingly used to understand plant strategies for growth and survival. However, it is unclear if frameworks developed at a global level can be applied in local communities and how well these frameworks—based largely on plant morphological traits—align with plant physiology and response to stress.

   We tested the ability of an integrated framework of plant form and function to characterise seedling trait variation and drought response among 22 grasses and forbs common in a semi‐arid grassland. We measured above‐ground and below‐ground traits, and survival to explore how drought response is linked to three trait dimensions (resource conservation, microbial collaboration, and plant size) associated with the framework as well as non‐morphological dimensions (e.g. physiological traits) that are under‐represented in global trait frameworks.

   We found support for three globally‐recognised axes representing trade‐offs in strategies associated with tissue investment (leaf nitrogen, leaf mass per area, root tissue density), below‐ground resource uptake (root diameter, specific root length), and size (shoot mass). However, in contrast to global patterns, above‐ground and below‐ground resource conservation gradients were oppositely aligned: root tissue density was positively correlated with leaf N rather than leaf mass per area. This likely reflects different investment strategies of annual and perennial herbaceous species, as fast‐growing annual species invested in lower density roots and less nitrogen‐rich leaves to maximise plant‐level carbon assimilation. Species with longer drought survival minimised water loss through small above‐ground size and low leaf‐level transpiration rates, and drought survival was best predicted by a principal component axis representing plant size.

   Contrary to our expectations, drought survival in seedlings did not align with the conservation or collaboration axes suggesting that seedlings with different functional strategies can achieve similar drought survival, as long as they minimise water loss. Our results also show that within local communities, expected trait relationships could be decoupled as some plant groups achieve similar performance through different trait combinations. The effectiveness of species mean trait values in predicting drought response highlights the value of trait‐based methods as a versatile tool for understanding ecological processes locally across various ecosystems.

   Read the freePlain Language Summaryfor this article on the Journal blog.

    

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4. Predictable Changes in Eelgrass Microbiomes with Increasing Wasting Disease Prevalence across 23° Latitude in the Northeastern Pacific

   https://doi.org/10.1128/msystems.00224-22  

   Beatty, Deanna S. ; Aoki, Lillian R. ; Rappazzo, Brendan ; Bergman, Chelsea ; Domke, Lia K. ; Duffy, J. Emmett ; Dubois, Katie ; Eckert, Ginny L. ; Gomes, Carla ; Graham, Olivia J. ; et al ( August 2022 , mSystems)

   Raina, Jean-Baptiste (Ed.)

   ABSTRACT Predicting outcomes of marine disease outbreaks presents a challenge in the face of both global and local stressors. Host-associated microbiomes may play important roles in disease dynamics but remain understudied in marine ecosystems. Host–pathogen–microbiome interactions can vary across host ranges, gradients of disease, and temperature; studying these relationships may aid our ability to forecast disease dynamics. Eelgrass, Zostera marina , is impacted by outbreaks of wasting disease caused by the opportunistic pathogen Labyrinthula zosterae . We investigated how Z. marina phyllosphere microbial communities vary with rising wasting disease lesion prevalence and severity relative to plant and meadow characteristics like shoot density, longest leaf length, and temperature across 23° latitude in the Northeastern Pacific. We detected effects of geography (11%) and smaller, but distinct, effects of temperature (30-day max sea surface temperature, 4%) and disease (lesion prevalence, 3%) on microbiome composition. Declines in alpha diversity on asymptomatic tissue occurred with rising wasting disease prevalence within meadows. However, no change in microbiome variability (dispersion) was detected between asymptomatic and symptomatic tissues. Further, we identified members of Cellvibrionaceae, Colwelliaceae, and Granulosicoccaceae on asymptomatic tissue that are predictive of wasting disease prevalence across the geographic range (3,100 kilometers). Functional roles of Colwelliaceae and Granulosicoccaceae are not known. Cellvibrionaceae, degraders of plant cellulose, were also enriched in lesions and adjacent green tissue relative to nonlesioned leaves. Cellvibrionaceae may play important roles in disease progression by degrading host tissues or overwhelming plant immune responses. Thus, inclusion of microbiomes in wasting disease studies may improve our ability to understand variable rates of infection, disease progression, and plant survival. IMPORTANCE The roles of marine microbiomes in disease remain poorly understood due, in part, to the challenging nature of sampling at appropriate spatiotemporal scales and across natural gradients of disease throughout host ranges. This is especially true for marine vascular plants like eelgrass ( Zostera marina ) that are vital for ecosystem function and biodiversity but are susceptible to rapid decline and die-off from pathogens like eukaryotic slime-mold Labyrinthula zosterae (wasting disease). We link bacterial members of phyllosphere tissues to the prevalence of wasting disease across the broadest geographic range to date for a marine plant microbiome-disease study (3,100 km). We identify Cellvibrionaceae, plant cell wall degraders, enriched (up to 61% relative abundance) within lesion tissue, which suggests this group may be playing important roles in disease progression. These findings suggest inclusion of microbiomes in marine disease studies will improve our ability to predict ecological outcomes of infection across variable landscapes spanning thousands of kilometers. 

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5. Environmental stress destabilizes microbial networks

   https://doi.org/10.1038/s41396-020-00882-x  

   Hernandez, Damian J. ; David, Aaron S. ; Menges, Eric S. ; Searcy, Christopher A. ; Afkhami, Michelle E. ( January 2021 , The ISME Journal)

   Environmental stress is increasing worldwide, yet we lack a clear picture of how stress disrupts the stability of microbial communities and the ecosystem services they provide. Here, we present the first evidence that naturally-occurring microbiomes display network properties characteristic of unstable communities when under persistent stress. By assessing changes in diversity and structure of soil microbiomes along 40 replicate stress gradients (elevation/water availability gradients) in the Florida scrub ecosystem, we show that: (1) prokaryotic and fungal diversity decline in high stress, and (2) two network properties of stable microbial communities—modularity and negative:positive cohesion—have a clear negative relationship with environmental stress, explaining 51–78% of their variation. Interestingly, pathogenic taxa/functional guilds decreased in relative abundance along the stress gradient, while oligotrophs and mutualists increased, suggesting that the shift in negative:positive cohesion could result from decreasing negative:positive biotic interactions consistent with the predictions of the Stress Gradient Hypothesis. Given the crucial role microbiomes play in ecosystem functions, our results suggest that, by limiting the compartmentalization of microbial associations and creating communities dominated by positive associations, increasing stress in the Anthropocene could destabilize microbiomes and undermine their ecosystem services.

    

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