More Like this

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. 

   more » « less
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)

   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.

    

   more » « less
3. 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)

   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.

    

   more » « less
4. A shift from exploitation to interference competition with increasing density affects population and community dynamics

   https://doi.org/10.1002/ece3.2284  

   Holdridge, Erica M. ; Cuellar‐Gempeler, Catalina ; terHorst, Casey P. ( July 2016 , Ecology and Evolution)

   Intraspecific competition influences population and community dynamics and occurs via two mechanisms. Exploitative competition is an indirect effect that occurs through use of a shared resource and depends on resource availability. Interference competition occurs by obstructing access to a resource and may not depend on resource availability. Our study tested whether the strength of interference competition changes with protozoa population density. We grew experimental microcosms of protozoa and bacteria under different combinations of protozoan density and basal resource availability. We then solved a dynamic predator–prey model for parameters of the functional response using population growth rates measured in our experiment. As population density increased, competition shifted from exploitation to interference, and competition was less dependent on resource levels. Surprisingly, the effect of resources was weakest when competition was the most intense. We found that at low population densities, competition was largely exploitative and resource availability had a large effect on population growth rates, but the effect of resources was much weaker at high densities. This shift in competitive mechanism could have implications for interspecific competition, trophic interactions, community diversity, and natural selection. We also tested whether this shift in the mechanism of competition with protozoa density affected the structure of the bacterial prey community. We found that both resources and protozoa density affected the structure of the bacterial prey community, suggesting that competitive mechanism may also affect trophic interactions.

    

   more » « less
5. Drought‐tolerant grassland species are generally more resistant to competition

   https://doi.org/10.1111/1365-2745.14243  

   Mount, Hailey E. ; Smith, Melinda D. ; Knapp, Alan K. ; Griffin‐Nolan, Robert J. ; Collins, Scott L. ; Atkins, David H. ; Stears, Alice E. ; Laughlin, Daniel C. ( February 2024 , Journal of Ecology)

   Plant populations are limited by resource availability and exhibit physiological trade‐offs in resource acquisition strategies. These trade‐offs may constrain the ability of populations to exhibit fast growth rates under water limitation and high cover of neighbours. However, traits that confer drought tolerance may also confer resistance to competition. It remains unclear how fitness responses to these abiotic conditions and biotic interactions combine to structure grassland communities and how this relationship may change along a gradient of water availability.

   To address these knowledge gaps, we estimated the low‐density growth rates of populations in drought conditions with low neighbour cover and in ambient conditions with average neighbour cover for 82 species in six grassland communities across the Central Plains and Southwestern United States. We assessed the relationship between population tolerance to drought and resistance to competition and determined if this relationship was consistent across a precipitation gradient. We also tested whether population growth rates could be predicted using plant functional traits.

   Across six sites, we observed a positive correlation between low‐density population growth rates in drought and in the presence of interspecific neighbours. This positive relationship was particularly strong in the grasslands of the northern Great Plains but weak in the most xeric grasslands. High leaf dry matter content and a low (more negative) leaf turgor loss point were associated with high population growth rates in drought and with neighbours in most grassland communities.

   Synthesis: A better understanding of how both biotic and abiotic factors impact population fitness provides valuable insights into how grasslands will respond to extreme drought. Our results advance plant strategy theory by suggesting that drought tolerance increases population resistance to interspecific competition in grassland communities. However, this relationship is not evident in the driest grasslands, where above‐ground competition is likely less important. Leaf dry matter content and turgor loss point may help predict which populations will establish and persist based on local water availability and neighbour cover, and these predictions can be used to guide the conservation and restoration of biodiversity in grasslands.

    

   more » « less