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1. Exometabolite Dynamics over Stationary Phase Reveal Strain-Specific Responses

   https://doi.org/10.1128/mSystems.00493-20  

   Chodkowski, John L.; Shade, Ashley (December 2020, mSystems)

   Gibbons, Sean M. (Ed.)

   ABSTRACT Microbial exponential growth is expected to occur infrequently in environments that have long periods of nutrient starvation punctuated by short periods of high nutrient flux. These conditions likely impose nongrowth states for microbes. However, nongrowth states are uncharacterized for the majority of environmental bacteria, especially in regard to exometabolite production. We compared exometabolites produced over stationary phase across three environmental bacteria: Burkholderia thailandensis E264 (ATCC 700388), Chromobacterium violaceum ATCC 31532, and Pseudomonas syringae pv. tomato DC3000 (ATCC BAA-871). We grew each strain in monoculture and investigated exometabolite dynamics from mid-exponential to stationary phases. We focused on exometabolites that were released into the medium and accumulated over 45 h, including approximately 20 h of stationary phase. We also analyzed transcripts (transcriptome sequencing [RNA-seq]) to interpret exometabolite output. We found that the majority of exometabolites released were strain specific, with a subset of identified exometabolites involved in both central and secondary metabolism. Transcript analysis supported that exometabolites were released from intact cells, as various transporters had either increased or consistent transcripts through time. Interestingly, we found that succinate was one of the most abundant identifiable exometabolites for all strains and that each strain rerouted their metabolic pathways involved in succinate production during stationary phase. These results show that nongrowth states can be metabolically dynamic and that environmental bacteria can enrich a minimal environment with diverse chemical compounds as a consequence of growth and postgrowth maintenance in stationary phase. This work provides insights into microbial community interactions via exometabolites under conditions of growth cessation or limitation. IMPORTANCE Nongrowth states are common for bacteria that live in environments that are densely populated and predominantly nutrient exhausted, and yet these states remain largely uncharacterized in cellular metabolism and metabolite output. Here, we investigated and compared stationary-phase exometabolites and RNA transcripts for each of three environmental bacterial strains. We observed that diverse exometabolites were produced and provide evidence that these exometabolites accumulate over time through release by intact cells. Additionally, each bacterial strain had a characteristic exometabolite profile and exhibited dynamics in exometabolite composition. This work affirms that stationary phase is metabolically dynamic, with each strain tested creating a unique chemical signature in the extracellular space and altering metabolism in stationary phase. These findings set the stage for understanding how bacterial populations can support surrounding neighbors in environments with prolonged nutrient exhaustion through exometabolite-mediated interspecies interactions. 

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2. Resource partitioning of phytoplankton metabolites that support bacterial heterotrophy

   https://doi.org/10.1038/s41396-020-00811-y  

   Ferrer-González, Frank Xavier; Widner, Brittany; Holderman, Nicole R.; Glushka, John; Edison, Arthur S.; Kujawinski, Elizabeth B.; Moran, Mary Ann (October 2020, The ISME Journal)

   Abstract The communities of bacteria that assemble around marine microphytoplankton are predictably dominated by Rhodobacterales, Flavobacteriales, and families within the Gammaproteobacteria. Yet whether this consistent ecological pattern reflects the result of resource-based niche partitioning or resource competition requires better knowledge of the metabolites linking microbial autotrophs and heterotrophs in the surface ocean. We characterized molecules targeted for uptake by three heterotrophic bacteria individually co-cultured with a marine diatom using two strategies that vetted the exometabolite pool for biological relevance by means of bacterial activity assays: expression of diagnostic genes and net drawdown of exometabolites, the latter detected with mass spectrometry and nuclear magnetic resonance using novel sample preparation approaches. Of the more than 36 organic molecules with evidence of bacterial uptake, 53% contained nitrogen (including nucleosides and amino acids), 11% were organic sulfur compounds (including dihydroxypropanesulfonate and dimethysulfoniopropionate), and 28% were components of polysaccharides (including chrysolaminarin, chitin, and alginate). Overlap in phytoplankton-derived metabolite use by bacteria in the absence of competition was low, and only guanosine, proline, and N-acetyl-d-glucosamine were predicted to be used by all three. Exometabolite uptake pattern points to a key role for ecological resource partitioning in the assembly marine bacterial communities transforming recent photosynthate. 

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3. Bacterial community function increases leaf growth in a pitcher plant experimental system

   https://doi.org/10.1128/msystems.01298-24  

   Bernardin, Jessica R; Young, Erica B; Gray, Sarah M; Bittleston, Leonora S (November 2024, mSystems)

   Nguyen, Nhu H (Ed.)

   ABSTRACT Across diverse ecosystems, bacteria and their hosts engage in complex relationships having negative, neutral, or positive interactions. However, the specific effects of leaf-associated bacterial community functions on plant growth are poorly understood. Although microbes can promote plant growth through various biochemical mechanisms, investigating the community’s functional contributions to plant growth remains to be explored. To address this gap, we characterized the relationships between bacterial community function and host plant growth in the purple pitcher plant (Sarracenia purpurea). The main aim of our research was to investigate how different bacterial community functions affect the growth and nutrient content in the plant. Previous research has suggested that microbial communities aid in prey decomposition and subsequent nutrient acquisition in carnivorous plants, includingS. purpurea. However, the specific functional roles of bacterial communities in plant growth and nutrient uptake are not well known. In this study, sterile, freshly opened pitchers were inoculated with three functionally distinct, pre-assembled bacterial communities. Bacterial community composition and function were measured over 8 weeks using physiological assays, metagenomics, and metatranscriptomics. Distinct community functions affected plant traits; a bacterial community enriched in decomposition was associated with larger leaves with almost double the biomass of control pitchers. Physiological differences in bacterial communities were supported by metatranscriptomics; for example, the bacterial community with the highest chitinase activity had greater expression of transcripts associated with chitinase enzymes. The relationship between bacterial community function and plant growth observed here indicates potential mechanisms, such as chitinase activity, for host-associated bacterial functions to support pitcher plant growth. IMPORTANCEThis study addresses a gap in understanding the relationships between bacterial community function and plant growth. We inoculated sterile, freshly opened pitcher plant leaves with three functionally distinct bacterial communities to uncover potential mechanisms through which bacterial functions support plant health and growth. Our findings demonstrate that distinct community functions significantly influence plant traits, with some bacterial communities supporting more plant growth than in control pitchers. These results highlight the ecological roles of microbial communities in plants and thus ecosystems and suggest that nutrient cycling is an important pathway through which microbes support host plant health. This research provides valuable insights into plant-microbe interactions and the effects of diverse microbial community functions. 

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4. From networks to mechanisms: A cross-scale analysis of bacterial - fungal interactions in fungal necromass

   Beatty, Briana (December 2024, University of Minnesota Graduate School)

   Microbial community dynamics are dependent on interactions between the community members, yet studies of interactions across domains and with multiple experimental approaches are lacking. In this study, we explored interactions between bacteria and fungi associated with decaying fungal necromass using both field-based co-occurrence networks and laboratory-based pairwise interactions. The majority of field-derived bacterial-fungal correlations were negative, suggesting a potentially competitive environment within necromass compared to other systems. Laboratory experiments consisted of bacteria most often reducing fungal growth, while the fungal effect on bacterial growth was more varied and dependent on bacterial taxa. However, these interactions were not consistently predicted by field correlations, highlighting a disconnect between field-based and direct experimental approaches. Our findings suggest that using co-occurrence networks alone to predict BFI outcomes could be misleading, emphasizing the need for more comprehensive, multi-method studies to capture the dynamic and context-dependent nature of microbial interactions. 

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5. Mechanistic approaches to investigate soil microbe‐mediated plant competition

   https://doi.org/10.1111/1365-2745.14156  

   Chung, Y. Anny; Ke, Po‐Ju; Adler, Peter B. (July 2023, Journal of Ecology)

   Abstract Interactions between plants and soil microbes can influence plant population dynamics and diversity in plant communities. Traditional theoretical paradigms view the microbial community as a black box with net effects described by phenomenological models.This approach struggles to quantify the importance of plant–microbe interactions relative to other competition and coexistence mechanisms and to explain context dependence in microbe effects.We argue that a mechanistic framework focused on microbial functional groups will lead to conceptual and empirical advances, as demonstrated by extending resource ratio theory to plant–microbe interactions. We review the diverse pathways by which different microbial functional groups can influence plant resource competition. Finally, we suggest approaches to link theory with observations to measure the key parameters of our framework.Synthesis: Our review highlights recent experimental advancements for uncovering microbial mechanisms that alter plant host resource competition and coexistence. We synthesize these mechanisms into a conceptual model that provides a framework for future experiments to investigate the importance of plant–microbe interactions in structuring plant populations and communities. 

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