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1. Diversification of Type VI Secretion System Toxins Reveals Ancient Antagonism among Bee Gut Microbes

   https://doi.org/10.1128/mBio.01630-17  

   Steele, Margaret I. ; Kwong, Waldan K. ; Whiteley, Marvin ; Moran, Nancy A. ; Lindow, Steven E. ( December 2017 , mBio)

   ABSTRACT Microbial communities are shaped by interactions among their constituent members. Some Gram-negative bacteria employ type VI secretion systems (T6SSs) to inject protein toxins into neighboring cells. These interactions have been theorized to affect the composition of host-associated microbiomes, but the role of T6SSs in the evolution of gut communities is not well understood. We report the discovery of two T6SSs and numerous T6SS-associated Rhs toxins within the gut bacteria of honey bees and bumble bees. We sequenced the genomes of 28 strains of Snodgrassella alvi , a characteristic bee gut microbe, and found tremendous variability in their Rhs toxin complements: altogether, these strains appear to encode hundreds of unique toxins. Some toxins are shared with Gilliamella apicola , a coresident gut symbiont, implicating horizontal gene transfer as a source of toxin diversity in the bee gut. We use data from a transposon mutagenesis screen to identify toxins with antibacterial function in the bee gut and validate the function and specificity of a subset of these toxin and immunity genes in Escherichia coli . Using transcriptome sequencing, we demonstrate that S. alvi T6SSs and associated toxins are upregulated in the gut environment. We find that S. alvi Rhs loci have a conserved architecture, consistent with the C-terminal displacement model of toxin diversification, with Rhs toxins, toxin fragments, and cognate immunity genes that are expressed and confer strong fitness effects in vivo . Our findings of T6SS activity and Rhs toxin diversity suggest that T6SS-mediated competition may be an important driver of coevolution within the bee gut microbiota. IMPORTANCE The structure and composition of host-associated bacterial communities are of broad interest, because these communities affect host health. Bees have a simple, conserved gut microbiota, which provides an opportunity to explore interactions between species that have coevolved within their host over millions of years. This study examined the role of type VI secretion systems (T6SSs)—protein complexes used to deliver toxic proteins into bacterial competitors—within the bee gut microbiota. We identified two T6SSs and diverse T6SS-associated toxins in bacterial strains from bees. Expression of these genes is increased in bacteria in the bee gut, and toxin and immunity genes demonstrate antibacterial and protective functions, respectively, when expressed in Escherichia coli . Our results suggest that coevolution among bacterial species in the bee gut has favored toxin diversification and maintenance of T6SS machinery, and demonstrate the importance of antagonistic interactions within host-associated microbial communities. 

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2. Structure and Long-Term Stability of the Microbiome in Diverse Diatom Cultures

   https://doi.org/10.1128/Spectrum.00269-21  

   Barreto Filho, Marcelo Malisano ; Walker, Melissa ; Ashworth, Matt P. ; Morris, J. Jeffrey ( September 2021 , Microbiology Spectrum)

   Gralnick, Jeffrey A. (Ed.)

   ABSTRACT Microalgal cultures are often maintained in xenic conditions, i.e., with associated bacteria, and many studies indicate that these communities both are complex and have significant impacts on the physiology of the target photoautotroph. Here, we investigated the structure and stability of microbiomes associated with a diverse sampling of diatoms during long-term maintenance in serial batch culture. We found that, counter to our initial expectation, evenness diversity increased with time since cultivation, driven by a decrease in dominance by the most abundant taxa in each culture. We also found that the site from which and time at which a culture was initially collected had a stronger impact on microbiome structure than the diatom species; however, some bacterial taxa were commonly present in most cultures despite having widely geographically separated collection sites. Our results support the conclusion that stochastic initial conditions (i.e., the local microbial community at the collection site) are important for the long-term structure of these microbiomes, but deterministic forces such as negative frequency dependence and natural selection exerted by the diatom are also at work. IMPORTANCE Natural microbial communities are extremely complex, with many more species coexisting in the same place than there are different resources to support them. Understanding the forces that allow this high level of diversity has been a central focus of ecological and evolutionary theory for many decades. Here, we used stock cultures of diatoms, which were maintained for years in continuous growth alongside populations of bacteria, as proxies for natural communities. We show that the bacterial communities remained relatively stable for years, and there is evidence that ecological forces worked to stabilize coexistence instead of favoring competition and exclusion. We also show evidence that, despite some important regional differences in bacterial communities, there was a globally present core microbiome potentially selected for in these diatom cultures. Understanding interactions between bacteria and diatoms is important both for basic ecological science and for practical science, such as industrial biofuel production. 

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3. Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods

   https://doi.org/10.1128/msystems.01519-21  

   Lewin, Gina R. ; Davis, Nicole M. ; McDonald, Bradon R. ; Book, Adam J. ; Chevrette, Marc G. ; Suh, Steven ; Boll, Ardina ; Currie, Cameron R. ( April 2022 , mSystems)

   Mackelprang, Rachel (Ed.)

   ABSTRACT The complexity of microbial communities hinders our understanding of how microbial diversity and microbe-microbe interactions impact community functions. Here, using six independent communities originating from the refuse dumps of leaf-cutter ants and enriched using the plant polymer cellulose as the sole source of carbon, we examine how changes in bacterial diversity and interactions impact plant biomass decomposition. Over up to 60 serial transfers (∼8 months) using Whatman cellulose filter paper, cellulolytic ability increased and then stabilized in four enrichment lines and was variable in two lines. Bacterial community characterization using 16S rRNA gene amplicon sequencing showed community succession differed between the highly cellulolytic enrichment lines and those that had slower and more variable cellulose degradation rates. Metagenomic and metatranscriptomic analyses revealed that Cellvibrio and/or Cellulomonas dominated each enrichment line and produced the majority of cellulase enzymes, while diverse taxa were retained within these communities over the duration of transfers. Interestingly, the less cellulolytic communities had a higher diversity of organisms competing for the cellulose breakdown product cellobiose, suggesting that cheating slowed cellulose degradation. In addition, we found competitive exclusion as an important factor shaping all of the communities, with a negative correlation of Cellvibrio and Cellulomonas abundance within individual enrichment lines and the expression of genes associated with the production of secondary metabolites, toxins, and other antagonistic compounds. Our results provide insights into how microbial diversity and competition affect the stability and function of cellulose-degrading communities. IMPORTANCE Microbial communities are a key driver of the carbon cycle through the breakdown of complex polysaccharides in diverse environments including soil, marine systems, and the mammalian gut. However, due to the complexity of these communities, the species-species interactions that impact community structure and ultimately shape the rate of decomposition are difficult to define. Here, we performed serial enrichment on cellulose using communities inoculated from leaf-cutter ant refuse dumps, a cellulose-rich environment. By concurrently tracking cellulolytic ability and community composition and through metagenomic and metatranscriptomic sequencing, we analyzed the ecological dynamics of the enrichment lines. Our data suggest that antagonism is prevalent in these communities and that competition for soluble sugars may slow degradation and lead to community instability. Together, these results help reveal the relationships between competition and polysaccharide decomposition, with implications in diverse areas ranging from microbial community ecology to cellulosic biofuels production. 

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4. Biotic and abiotic drivers of plant–pollinator community assembly across wildfire gradients

   https://doi.org/10.1111/1365-2745.13530  

   LaManna, Joseph A. ; Burkle, Laura A. ; Belote, R. Travis ; Myers, Jonathan A. ; Bartomeus, ed., Ignasi ( November 2020 , Journal of Ecology)

   Understanding how abiotic disturbance and biotic interactions determine pollinator and flowering‐plant diversity is critically important given global climate change and widespread pollinator declines. To predict responses of pollinators and flowering‐plant communities to changes in wildfire disturbance, a mechanistic understanding of how these two trophic levels respond to wildfire severity is needed.

   We compared site‐to‐site variation in community composition (β‐diversity), species richness and abundances of pollinators and flowering plants among landscapes with no recent wildfire (unburned), mixed‐severity wildfire and high‐severity wildfire in three sites across the Northern Rockies Ecoregion, USA. We used variation partitioning to assess the relative contributions of wildfire, other abiotic variables (climate, soils and topography) and biotic associations among plant and pollinator composition to community assembly of both trophic levels.

   Wildfire disturbance generally increased species richness and total abundance, but decreasedβ‐diversity, of both pollinators and flowering plants. However, reductions inβ‐diversity from wildfire appeared to result from increased abundances following fires, resulting in higher local species richness of pollinators and flowers in burned than unburned landscapes. After accounting for differences in abundance, standardized effect sizes ofβ‐diversity were higher in burned than unburned landscapes, suggesting that wildfire enhances non‐random assortment of pollinator and flowering‐plant species among local communities.

   Wildfire disturbance mediated the relative importance of mutualistic associations toβ‐diversity of pollinators and flowering plants. The influence of pollinatorβ‐diversity on flowering‐plantβ‐diversity increased with wildfire severity, whereas the influence of flowering‐plantβ‐diversity on pollinatorβ‐diversity was greater in mixed‐severity than high‐severity wildfire or unburned landscapes. Moreover, biotic associations among pollinator and plant species explained substantial variation inβ‐diversity of both trophic levels beyond what could be explained by wildfire and all other abiotic and spatial factors combined.

   Synthesis. Wildfire disturbance and plant–pollinator interactions both strongly influenced the assembly of pollinator and flowering‐plant communities at local and regional scales. However, biotic interactions were generally more important drivers of community assembly in disturbed than undisturbed landscapes. As wildfire regimes continue to change globally, predicting its effects on biodiversity will require a deeper understanding of the ecological processes that mediate biotic interactions among linked trophic levels.

    

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5. Emerging palaeoecological frameworks for elucidating plant dynamics in response to fire and other disturbance

   https://doi.org/10.1111/geb.13416  

   Napier, Joseph D. ; Chipman, Melissa L. ( October 2021 , Global Ecology and Biogeography)

   Rapid climate change is altering plant communities around the globe fundamentally. Despite progress in understanding how plants respond to these climate shifts, accumulating evidence suggests that disturbance could not only modify expected plant responses but, in some cases, have larger impacts on compositional shifts than climate change. Climate‐driven disturbances are becoming increasingly common in many biomes and are key drivers of vegetation dynamics at both species and community levels. Palaeoecological records provide valuable observational windows for elucidating the long‐term impacts of these disturbances on plant dynamics; however, sparse resolution and difficulty in disentangling drivers of change limit our ability to understand the impact of disturbance on plant communities. In this targeted review, we highlight emerging opportunities in palaeoecology to advance our understanding about how disturbance, especially fire, impacts the ecological and evolutionary dynamics of terrestrial plant communities.

   Global examples, with many from North America.

   We propose a set of palaeoecological and integrative approaches that could greatly enhance our understanding of how disturbance regimes influence global plant dynamics. Specifically, we identify four future study areas: (1) focus on palaeoecological disturbance proxies beyond fire and leverage multi proxy research to examine the influence of interacting disturbances on plant community dynamics; (2) use advances in disturbance and vegetation reconstructions, including ancient sedimentary DNA, to provide the spatial, temporal and taxonomic resolution needed to resolve the relationship between changing disturbance regimes and corresponding shifts in plant community composition; (3) integrate palaeoecological, archaeological and Indigenous knowledge to disentangle the complex interplay between climate, human land use, fire and vegetation structure; and (4) apply “functional palaeoecology” and the synergy between palaeoecology and genetics to understand how fire disturbance has served as a long‐standing selective agent on plants. These frameworks could increase the resolution of disturbance‐driven plant dynamics, potentially providing valuable information for future management.

    

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