Abstract
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.
Highlights
In pitcher plants, sequencing has provided a detailed appreciation for microbial diversity and functions in the food web (Boynton, 2012; Gray et al, 2012; Paisie et al, 2014; Armitage, 2017; Bittleston et al, 2018; Canter et al, 2018; Grothjan and Young, 2019). For this model system to help us understand microbial functions in food web ecology, and for broader understanding of plant host microbiome associations, we need more information about how microbial taxa are recruited to pitcher plant communities, and which sources of bacteria are most important in contributing functionally important taxa (Siragusa et al, 2007; Koopman and Carstens, 2011; Gray et al, 2012)
To address the gaps in our understanding of microbial recruitment to pitcher communities, this study examined communities hosted by S. purpurea pitchers, in a controlled greenhouse environment, applying bacterial gene sequencing and functional predictions, measures of bacterial cell abundance and hydrolytic enzyme activity, to address three key research questions: 1. How do potential sources of bacteria affect the development of the bacterial community within pitchers? This was examined as changes in community composition in pitcher treatments which excluded different potential sources of bacteria, comparing with an established microbial community from field plants
Acidobacteriaceae was common at most timepoints in living pitcher treatments but nearly absent from artificial pitchers” (ART) pitchers and Microbacteriaceae and Rhodanobacteraceae were more common in living pitcher treatments (p < 0.045, p < 0.001)
Summary
The processes defining how host-associated microbial communities develop and assemble are complex and not well understood. In pitcher plants, sequencing has provided a detailed appreciation for microbial diversity and functions in the food web (Boynton, 2012; Gray et al, 2012; Paisie et al, 2014; Armitage, 2017; Bittleston et al, 2018; Canter et al, 2018; Grothjan and Young, 2019). For this model system to help us understand microbial functions in food web ecology, and for broader understanding of plant host microbiome associations, we need more information about how microbial taxa are recruited to pitcher plant communities, and which sources of bacteria are most important in contributing functionally important taxa (Siragusa et al, 2007; Koopman and Carstens, 2011; Gray et al, 2012)
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