Understanding microbial roles in ecosystem function requires integrating microscopic processes into food webs. The carnivorous pitcher plant,
- Award ID(s):
- 2025337
- NSF-PAR ID:
- 10386942
- Date Published:
- Journal Name:
- Frontiers in Microbiology
- Volume:
- 13
- ISSN:
- 1664-302X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Sarracenia purpurea , offers a tractable study system where diverse food webs of macroinvertebrates and microbes facilitate digestion of captured insect prey, releasing nutrients supporting the food web and host plant. However, how interactions between these macroinvertebrate and microbial communities contribute to ecosystem functions remains unclear. We examined the role of the pitcher plant mosquito,Wyeomyia smithii , in top‐down control of the composition and function of pitcher plant microbial communities. Mosquito larval abundance was enriched or depleted across a natural population ofS. purpurea pitchers over a 74‐day field experiment. Bacterial community composition and microbial community function were characterized by 16S rRNA amplicon sequencing and profiling of carbon substrate use, bulk metabolic rate, hydrolytic enzyme activity, and macronutrient pools. Bacterial communities changed from pitcher opening to maturation, but larvae exerted minor effects on high‐level taxonomic composition. Higher larval abundance was associated with lower diversity communities with distinct functions and elevated nitrogen availability. Treatment‐independent clustering also supported roles for larvae in curating pitcher microbial communities through shifts in community diversity and function. These results demonstrate top‐down control of microbial functions in an aquatic microecosystem. -
Summary Plant‐associated microbial communities can profoundly affect plant health and success, and research is still uncovering factors driving the assembly of these communities. Here, we examine how geography versus host species affects microbial community structure and differential abundances of individual taxa. We use metabarcoding to characterize the bacteria and eukaryotes associated with five, often co‐occurring species of
Sarracenia pitcher plants (Sarraceniaceae) and three natural hybrids along the longitudinal gradient of the U.S. Gulf Coast, as well as samples fromS .purpurea in Massachusetts. To tease apart the effects of geography versus host species, we focus first on sites with co‐occurring species and then on species located across different sites. Our analyses show that bacterial and eukaryotic community structures are clearly and consistently influenced by host species identity, with geographic factors also playing a role. Naturally occurring hybrids appear to also host unique communities, which are in some ways intermediate between their parent species. We see significant effects of geography (site and longitude), but these generally explain less of the variation among pitcher communities. Overall, inSarracenia pitchers, host plant phenotype significantly affects the pitcher microbiomes and other associated organisms. -
Abstract The spatial distribution of predators can affect both the distribution and diversity of their prey. Therefore, differences in predator dispersal ability that affect their spatial distribution, could also affect prey communities. Here, we use the microbial communities within pitcher plant leaves as a model system to test the relationship between predator (protozoa) dispersal ability and distribution, and its consequences for prey (bacteria) diversity and composition. We hypothesized that limited predator dispersal results in clustered distributions and heterogeneous patches for prey species, whereas wide predator dispersal and distribution could homogenize prey metacommunities. We analyzed the distribution of two prominent bacterivore protozoans from a 2‐year survey of an intact field of
Sarracenia purpurea pitcher plants, and found a clustered distribution ofTetrahymena and homogeneous distribution ofPoterioochromonas . We manipulated the sources of protozoan colonists and recorded protozoan recruitment and bacterial diversity in target leaves in a field experiment. We found the large ciliate,Tetrahymena , was dispersal limited and occupied few leaves, whereas the small flagellatePoterioochromonas was widely dispersed. However, the bacterial communities these protozoans feed on was unaffected by clustering ofTetrahymena , but likely influenced byPoterioochromonas and other bacterivores dispersing in the field. We propose that bacterial communities in this system are structured by a combination of well dispersed bacterivores, bacterial dispersal, and bottom‐up mechanisms. Clustered predators could become strong drivers of prey communities if they were specialists or keystone predators, or if they exerted a dominant influence on other predators in top‐down controlled systems. Linking dispersal ability within trophic levels and its consequences for trophic dynamics can lead to a more robust perspective on trophic metacommunities. -
The Albany pitcher plant, Cephalotus follicularis , has evolved cup-shaped leaves and a carnivorous habit completely independently from other lineages of pitcher plants. It is the only species in the family Cephalotaceae and is restricted to a small region of Western Australia. Here, we used metabarcoding to characterize the bacterial and eukaryotic communities living in C. follicularis pitchers at two different sites. Bacterial and eukaryotic communities were correlated in both richness and composition; however, the factors associated with richness were not the same across bacteria and eukaryotes, with bacterial richness differing with fluid color, and eukaryotic richness differing with the concentration of DNA extracted from the fluid, a measure roughly related to biomass. For turnover in composition, the variation in both bacterial and eukaryotic communities primarily differed with fluid acidity, fluid color, and sampling site. We compared C. follicularis -associated community diversity with that of Australian Nepenthes mirabilis , as well as a global comparison of Southeast Asian Nepenthes and North American Sarracenia . Our results showed similarity in richness with communities from other pitcher plants, and specific bacterial taxa shared among all three independent lineages of pitcher plants. Overall, we saw convergence in richness and particular clades colonizing pitcher plants around the world, suggesting that these highly specialized habitats select for certain numbers and types of inhabitants.more » « less
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Abstract Background The leaves of carnivorous pitcher plants harbor diverse communities of inquiline species, including bacteria and larvae of the pitcher plant mosquito (
Wyeomyia smithii ), which aid the plant by processing captured prey. Despite the growing appreciation for this microecosystem as a tractable model in which to study food web dynamics and the moniker ofW. smithii as a ‘keystone predator’, very little is known about microbiota acquisition and assembly inW. smithii mosquitoes or the impacts ofW. smithii -microbiota interactions on mosquito and/or plant fitness.Results In this study, we used high throughput sequencing of bacterial 16S rRNA gene amplicons to characterize and compare microbiota diversity in field- and laboratory-derived
W. smithii larvae. We then conducted controlled experiments in the laboratory to better understand the factors shaping microbiota acquisition and persistence across theW. smithii life cycle. Methods were also developed to produce axenic (microbiota-free)W. smithii larvae that can be selectively recolonized with one or more known bacterial species in order to study microbiota function. Our results support a dominant role for the pitcher environment in shaping microbiota diversity inW. smithii larvae, while also indicating that pitcher-associated microbiota can persist in and be dispersed by adultW. smithii mosquitoes. We also demonstrate the successful generation of axenicW. smithii larvae and report variable fitness outcomes in gnotobiotic larvae monocolonized by individual bacterial isolates derived from naturally occurring pitchers in the field.Conclusions This study provides the first information on microbiota acquisition and assembly in
W. smithii mosquitoes. This study also provides the first evidence for successful microbiota manipulation in this species. Altogether, our results highlight the value of such methods for studying host-microbiota interactions and lay the foundation for future studies to understand howW. smithii -microbiota interactions shape the structure and stability of this important model ecosystem.