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1. Microbiome metabolic capacity is buffered against phylotype losses by functional redundancy

   https://doi.org/10.1128/aem.02368-24  

   Cross, Kayla; Beckman, Noelle; Jahnes, Benjamin; Sabree, Zakee L (February 2025, Applied and Environmental Microbiology)

   Rudi, Knut (Ed.)

   ABSTRACT Many animals contain a species-rich and diverse gut microbiota that likely contributes to several host-supportive services that include diet processing and nutrient provisioning. Loss of microbiome taxa and their associated metabolic functions as result of perturbations may result in loss of microbiome-level services and reduction of metabolic capacity. If metabolic functions are shared by multiple taxa (i.e., functional redundancy), including deeply divergent lineages, then the impact of taxon/function losses may be dampened. We examined to what degree alterations in phylotype diversity impact microbiome-level metabolic capacity. Feeding two nutritionally imbalanced diets to omnivorousPeriplaneta americanaover 8 weeks reduced the diversity of their phylotype-rich gut microbiomes by ~25% based on 16S rRNA gene amplicon sequencing, yet PICRUSt2-inferred metabolic pathway richness was largely unaffected due to their being polyphyletic. We concluded that the nonlinearity between taxon and metabolic functional losses is due to microbiome members sharing many well-characterized metabolic functions, with lineages remaining after perturbation potentially being capable of preventing microbiome “service outages” due to functional redundancy. IMPORTANCEDiet can affect gut microbiome taxonomic composition and diversity, but its impacts on community-level functional capabilities are less clear. Host health and fitness are increasingly being linked to microbiome composition and further modeling of the relationship between microbiome taxonomic and metabolic functional capability is needed to inform these linkages. Invertebrate animal models like the omnivorous American cockroach are ideal for this inquiry because they are amenable to various diets and provide high replicates per treatment at low costs and thus enabling rigorous statistical analyses and hypothesis testing. Microbiome taxonomic composition is diet-labile and diversity was reduced after feeding on unbalanced diets (i.e., post-treatment), but the predicted functional capacities of the post-treatment microbiomes were less affected likely due to the resilience of several abundant taxa surviving the perturbation as well as many metabolic functions being shared by several taxa. These results suggest that both taxonomic and functional profiles should be considered when attempting to infer how perturbations are altering gut microbiome services and possible host outcomes. 

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2. The endohyphal microbiome: current progress and challenges for scaling down integrative multi-omic microbiome research

   https://doi.org/10.1186/s40168-023-01634-7  

   Kelliher, Julia M.; Robinson, Aaron J.; Longley, Reid; Johnson, Leah Y.; Hanson, Buck T.; Morales, Demosthenes P.; Cailleau, Guillaume; Junier, Pilar; Bonito, Gregory; Chain, Patrick S. (December 2023, Microbiome)

   Abstract As microbiome research has progressed, it has become clear that most, if not all, eukaryotic organisms are hosts to microbiomes composed of prokaryotes, other eukaryotes, and viruses. Fungi have only recently been considered holobionts with their own microbiomes, as filamentous fungi have been found to harbor bacteria (including cyanobacteria), mycoviruses, other fungi, and whole algal cells within their hyphae. Constituents of this complex endohyphal microbiome have been interrogated using multi-omic approaches. However, a lack of tools, techniques, and standardization for integrative multi-omics for small-scale microbiomes (e.g., intracellular microbiomes) has limited progress towards investigating and understanding the total diversity of the endohyphal microbiome and its functional impacts on fungal hosts. Understanding microbiome impacts on fungal hosts will advance explorations of how “microbiomes within microbiomes” affect broader microbial community dynamics and ecological functions. Progress to date as well as ongoing challenges of performing integrative multi-omics on the endohyphal microbiome is discussed herein. Addressing the challenges associated with the sample extraction, sample preparation, multi-omic data generation, and multi-omic data analysis and integration will help advance current knowledge of the endohyphal microbiome and provide a road map for shrinking microbiome investigations to smaller scales. 

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3. Long-Term Nutrient Enrichment of an Oligotroph-Dominated Wetland Increases Bacterial Diversity in Bulk Soils and Plant Rhizospheres

   https://doi.org/10.1128/mSphere.00035-20  

   Bledsoe, Regina B.; Goodwillie, Carol; Peralta, Ariane L. (June 2020, mSphere)

   Campbell, Barbara J. (Ed.)

   ABSTRACT In nutrient-limited conditions, plants rely on rhizosphere microbial members to facilitate nutrient acquisition, and in return, plants provide carbon resources to these root-associated microorganisms. However, atmospheric nutrient deposition can affect plant-microbe relationships by changing soil bacterial composition and by reducing cooperation between microbial taxa and plants. To examine how long-term nutrient addition shapes rhizosphere community composition, we compared traits associated with bacterial (fast-growing copiotrophs, slow-growing oligotrophs) and plant (C 3 forb, C 4 grass) communities residing in a nutrient-poor wetland ecosystem. Results revealed that oligotrophic taxa dominated soil bacterial communities and that fertilization increased the presence of oligotrophs in bulk and rhizosphere communities. Additionally, bacterial species diversity was greatest in fertilized soils, particularly in bulk soils. Nutrient enrichment (fertilized versus unfertilized) and plant association (bulk versus rhizosphere) determined bacterial community composition; bacterial community structure associated with plant functional group (grass versus forb) was similar within treatments but differed between fertilization treatments. The core forb microbiome consisted of 602 unique taxa, and the core grass microbiome consisted of 372 unique taxa. Forb rhizospheres were enriched in potentially disease-suppressive bacterial taxa, and grass rhizospheres were enriched in bacterial taxa associated with complex carbon decomposition. Results from this study demonstrate that fertilization serves as a strong environmental filter on the soil microbiome, which leads to distinct rhizosphere communities and can shift plant effects on the rhizosphere microbiome. These taxonomic shifts within plant rhizospheres could have implications for plant health and ecosystem functions associated with carbon and nitrogen cycling. IMPORTANCE Over the last century, humans have substantially altered nitrogen and phosphorus cycling. Use of synthetic fertilizer and burning of fossil fuels and biomass have increased nitrogen and phosphorus deposition, which results in unintended fertilization of historically low-nutrient ecosystems. With increased nutrient availability, plant biodiversity is expected to decline, and the abundance of copiotrophic taxa is anticipated to increase in bacterial communities. Here, we address how bacterial communities associated with different plant functional types (forb, grass) shift due to long-term nutrient enrichment. Unlike other studies, results revealed an increase in bacterial diversity, particularly of oligotrophic bacteria in fertilized plots. We observed that nutrient addition strongly determines forb and grass rhizosphere composition, which could indicate different metabolic preferences in the bacterial communities. This study highlights how long-term fertilization of oligotroph-dominated wetlands could alter diversity and metabolism of rhizosphere bacterial communities in unexpected ways. 

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4. Lake Sediment Methane Responses to Organic Matter are Related to Microbial Community Composition in Experimental Microcosms

   https://doi.org/10.3389/fenvs.2022.834829  

   Bertolet, Brittni L.; Koepfli, Cristian; Jones, Stuart E. (March 2022, Frontiers in Environmental Science)

   Lake sediment microbial communities mediate carbon diagenesis. However, microbial community composition is variable across lakes, and it is still uncertain how variation in community composition influences sediment responses to environmental change. Sediment methane (CH 4 ) production has been shown to be substantially elevated by increased lake primary productivity and organic matter supply. However, the magnitude of the response of CH 4 production varies across lakes, and recent studies suggest a role for the microbial community in mediating this response. Here, we conducted sediment incubation experiments across 22 lakes to determine whether variation in sediment microbial community composition is related to the response of sediment CH 4 production to increases in organic matter. We sampled the 22 lakes across a gradient of pH in order to investigate lakes with variable sediment microbial communities. We manipulated the incubations with additions of dried algal biomass and show that variation in the response of CH 4 production to changes in organic matter supply is significantly correlated with metrics of sediment microbial community composition. Specifically, the diversity and richness of the non-methanogen community was most predictive of sediment CH 4 responses to organic matter additions. Additionally, neither metrics of microbial abundance nor preexisting organic matter availability explained meaningful variation in the response. Thus, our results provide experimental support that differences in sediment microbial communities influences CH 4 production responses to changes in organic matter availability. 

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5. Structuring Life After Death: Plant Leachates Promote CO2 Uptake by Regulating Microbial Biofilm Interactions in a Northern Peatland Ecosystem

   https://doi.org/10.1007/s10021-023-00820-w  

   Rober, Allison R.; Lankford, Allyson J.; Kane, Evan S.; Turetsky, Merritt R.; Wyatt, Kevin H. (January 2023, Ecosystems)

   Abstract Shifts in plant functional groups associated with climate change have the potential to influence peatland carbon storage by altering the amount and composition of organic matter available to aquatic microbial biofilms. The goal of this study was to evaluate the potential for plant subsidies to regulate ecosystem carbon flux (CO₂) by governing the relative proportion of primary producers (microalgae) and heterotrophic decomposers (heterotrophic bacteria) during aquatic biofilm development in an Alaskan fen. We evaluated biofilm composition and CO₂flux inside mesocosms with and without nutrients (both nitrogen and phosphorus), organic carbon (glucose), and leachates from common peatland plants (moss, sedge, shrub, horsetail). Experimental mesocosms were exposed to either natural sunlight or placed under a dark canopy to evaluate the response of decomposers to nutrients and carbon subsidies with and without algae, respectively. Algae were limited by inorganic nutrients and heterotrophic bacteria were limited by organic carbon. The quality of organic matter varied widely among plants and leachate nutrient content, more so than carbon quality, influenced biofilm composition. By alleviating nutrient limitation of algae, plant leachates shifted the biofilm community toward autotrophy in the light-transparent treatments, resulting in a significant reduction in CO₂emissions compared to the control. Without the counterbalance from algal photosynthesis, a heterotrophic biofilm significantly enhanced CO₂emissions in the presence of plant leachates in the dark. These results show that plants not only promote carbon uptake directly through photosynthesis, but also indirectly through a surrogate, the phototrophic microbes. 

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