ABSTRACT We examined how larvae of Culex restuans mosquito influences the bacterial abundance, composition and diversity in simulated container aquatic habitats. The microbiota of Cx. restuans larvae were also characterized and compared to those of their larval habitats. The presence of Cx. restuans larvae altered the bacterial community composition and reduced the bacterial abundance, diversity and richness. Azohydromonas sp., Delftia sp., Pseudomonas sp., Zooglea sp., unclassified Enterobacteriaceae and unclassified Bacteroidales were suppressed while Prosthecobacter sp., Hydrogenaphaga sp., Clostridium sp., unclassified Clostridiaceae and Chryseobacterium sp. were enhanced in the presence of Cx. restuans larvae. Cx. restuans larvae harbored distinct and less diverse bacterial community compared to their larval habitats. These findings demonstrate that Cx. restuans larvae play a key role in structuring the microbial communities in container aquatic habitats and may lower the nutritional quality and alter the decomposition process and food web dynamics in these aquatic systems. The findings also demonstrate that mosquito larvae are highly selective of the bacterial taxa from the larval environment that colonize their bodies. These findings provide new opportunities for more focused studies to identify the specific bacterial taxa that serve as food for mosquito larvae and those that could be harnessed for disease control.
more »
« less
An inquiline mosquito modulates microbial diversity and function in an aquatic microecosystem
Understanding microbial roles in ecosystem function requires integrating microscopic processes into food webs. The carnivorous pitcher plant,
- Award ID(s):
- 2019368
- NSF-PAR ID:
- 10494177
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 33
- Issue:
- 7
- ISSN:
- 0962-1083
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Processes influencing recruitment of diverse bacteria to plant microbiomes remain poorly understood. In the carnivorous pitcher plant Sarracenia purpurea model system, individual pitchers open to collect rainwater, invertebrates and a diverse microbial community, and this detrital food web is sustained by captured insect prey. This study examined how potential sources of bacteria affect the development of the bacterial community within pitchers, how the host plant tissue affects community development and how established vs. assembling communities differ. In a controlled greenhouse experiment, seven replicate pitchers were allocated to five treatments to exclude specific bacterial sources or host tissue: milliQ water only, milliQ + insect prey, rainwater + prey, established communities + prey, artificial pitchers with milliQ + prey. Community composition and functions were examined over 8–40 weeks using bacterial gene sequencing and functional predictions, measurements of cell abundance, hydrolytic enzyme activity and nutrient transformations. Distinct community composition and functional differences between artificial and real pitchers confirm an important influence of host plant tissue on community development, but also suggest this could be partially related to host nutrient uptake. Significant recruitment of bacteria to pitchers from air was evident from many taxa common to all treatments, overlap in composition between milliQ, milliQ + prey, and rainwater + prey treatments, and few taxa unique to milliQ only pitchers. Community functions measured as hydrolytic enzyme (chitinase, protease) activity suggested a strong influence of insect prey additions and were linked to rapid transformation of insect nutrients into dissolved and inorganic sources. Bacterial taxa found in 6 of 7 replicate pitchers within treatments, the “core microbiome” showed tighter successional trajectories over 8 weeks than all taxa. Established pitcher community composition was more stable over 8 weeks, suggesting a diversity-stability relationship and effect of microinvertebrates on bacteria. This study broadly demonstrates that bacterial composition in host pitcher plants is related to both stochastic and specific bacterial recruitment and host plants influence microbial selection and support microbiomes through capture of insect prey.more » « less
-
more » « less
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. -
null (Ed.)Abstract Mosquito bacterial communities are essential in mosquito biology, and knowing the factors shaping these bacterial communities is critical to their application in mosquito-borne disease control. This study investigated how the larval environment influences the bacterial communities of larval stages of two container-dwelling mosquito species, Aedes triseriatus, and Aedes japonicus. Larval and water samples were collected from tree holes and used tires at two study sites, and their bacteria characterized through MiSeq sequencing of the 16S rRNA gene. Bacterial richness was highest in Ae. japonicus , intermediate in Ae. triseriatus , and lowest in water samples. Dysgonomonas was the dominant bacterial taxa in Ae. triseriatus larvae; the unclassified Comamonadaceae was dominant in water samples from waste tires, while Mycobacterium and Carnobacterium , dominated Ae. japonicus . The two mosquito species harbored distinct bacterial communities that were different from those of the water samples. The bacterial communities also clustered by habitat type (used tires vs. tree holes) and study site. These findings demonstrate that host species, and the larval sampling environment are important determinants of a significant component of bacterial community composition and diversity in mosquito larvae and that the mosquito body may select for microbes that are generally rare in the larval environment.more » « less
-
more » « less
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.
