skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Substrate complexity buffers negative interactions in a synthetic community of leaf litter degraders
Abstract Leaf litter microbes collectively degrade plant polysaccharides, influencing land–atmosphere carbon exchange. An open question is how substrate complexity—defined as the structure of the saccharide and the amount of external processing by extracellular enzymes—influences species interactions. We tested the hypothesis that monosaccharides (i.e. xylose) promote negative interactions through resource competition, and polysaccharides (i.e. xylan) promote neutral or positive interactions through resource partitioning or synergism among extracellular enzymes. We assembled a three-species community of leaf litter-degrading bacteria isolated from a grassland site in Southern California. In the polysaccharide xylan, pairs of species stably coexisted and grew equally in coculture and in monoculture. Conversely, in the monosaccharide xylose, competitive exclusion and negative interactions prevailed. These pairwise dynamics remained consistent in a three-species community: all three species coexisted in xylan, while only two species coexisted in xylose, with one species capable of using peptone. A mathematical model showed that in xylose these dynamics could be explained by resource competition. Instead, the model could not predict the coexistence patterns in xylan, suggesting other interactions exist during biopolymer degradation. Overall, our study shows that substrate complexity influences species interactions and patterns of coexistence in a synthetic microbial community of leaf litter degraders.  more » « less
Award ID(s):
2308342
PAR ID:
10529484
Author(s) / Creator(s):
; ; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
FEMS Microbiology Ecology
Volume:
100
Issue:
8
ISSN:
1574-6941
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Allelopathy (i.e., chemical interaction among species) was originally conceived as inclusive of positive and negative effects of plants on other plants, and we adopt this view. Most studies of allelopathy have been phenomenological, but we focus on studies that have explored the ecological significance of this interaction. The literature suggests that studies of allelopathy have been particularly important for three foci in ecology: species distribution, conditionality of interactions, and maintenance of species diversity. There is evidence that allelopathy influences local distributions of plant species around the world. Allelopathic conditionality appears to arise through coevolution, and this is a mechanism for plant invasions. Finally, allelopathy promotes species coexistence via intransitive competition, modifications of direct interactions, and (co)evolution. Recent advances additionally suggest that coexistence might be favored through biochemical recognition. The preponderance of phenomenological studies notwithstanding, allelopathy has broad ecological consequences. 
    more » « less
  2. Summary Spring phytoplankton blooms in temperate environments contribute disproportionately to global marine productivity. Bloom‐derived organic matter, much of it occurring as polysaccharides, fuels biogeochemical cycles driven by interacting autotrophic and heterotrophic communities. We tracked changes in the mode of polysaccharide utilization by heterotrophic bacteria during the course of a diatom‐dominated bloom in the German Bight, North Sea. Polysaccharides can be taken up in a ‘selfish’ mode, where initial hydrolysis is coupled to transport into the periplasm, such that little to no low‐molecular weight (LMW) products are externally released to the environment. Alternatively, polysaccharides hydrolyzed by cell‐surface attached or free extracellular enzymes (external hydrolysis) yield LMW products available to the wider bacterioplankton community. In the early bloom phase, selfish activity was accompanied by low extracellular hydrolysis rates of a few polysaccharides. As the bloom progressed, selfish uptake increased markedly, and external hydrolysis rates increased, but only for a limited range of substrates. The late bloom phase was characterized by high external hydrolysis rates of a broad range of polysaccharides and reduced selfish uptake of polysaccharides, except for laminarin. Substrate utilization mode is related both to substrate structural complexity and to the bloom‐stage dependent composition of the heterotrophic bacterial community. 
    more » « less
  3. 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. 
    more » « less
  4. null (Ed.)
    Abstract Species that use the same resources present a paradox for understanding their coexistence. This is especially true for cryptic species because they are phenotypically similar. We examined how competition affects food-resource use in three cryptic species of Hyalella Smith, 1874, a freshwater-amphipod genus. We hypothesized that competitively inferior species would use high-quality algae patches when alone and competitively superior species would displace inferior species to low-quality patches. We compared use of foraging patches varying in algal content (i.e., quality) when species were alone or with another species. Our results showed that the competitively inferior species spent more time on the low-quality patch in the presence of the competitively superior species, but the behavior of the competitively superior species was independent of heterospecifics. This study provides insight into the role of interspecific competition in shaping resource use and patterns of coexistence in nature. 
    more » « less
  5. Abstract Understanding the drivers and impacts of spatiotemporal variation in species abundance on community trajectories is key to understanding the factors contributing to ecosystem resilience. Temporal variation in species trajectories across patches can provide compensation for species loss and can influence successional patterns. However, little is known about the underlying mechanisms that lead to patterns of species or spatial compensation and how those patterns may be mediated by consumer–resource relationships. Here we describe an experiment testing whether habitat attributes (e.g., structural complexity and spatial heterogeneity) mediate the effects of herbivory on tropical marine macroalgal communities by reducing accessibility and detectability, respectively, leading to variable trajectories among algal species at community (within patch) and metacommunity (i.e., among patch) scales. Reduced accessibility (greater habitat complexity) decreased the effects of herbivory (i.e., depressed consumption rate, increased algal species richness), and both accessibility and detectability (spatial heterogeneity) influenced algal community structure. Moreover, decreased accessibility at the community scale and a mosaic of accessibility at the metacommunity scale led to variation in community assembly. We suggest that habitat attributes can be important influencers of consumer–resource interactions on coral reefs, which in turn can increase species diversity, promote species succession, and enhance stability in algal metacommunities. 
    more » « less