Predator identity more than predator richness structures aquatic microbial assemblages in Sarracenia purpurea leaves

Abstract

The importance of predators in influencing community structure is a well-studied area of ecology. However, few studies test ecological hypotheses of predation in multi-predator microbial communities. The phytotelmic community found within the water-filled leaves of the pitcher plant, Sarracenia purpurea, exhibits a simple trophic structure that includes multiple protozoan predators and microbial prey. Using this system, we sought to determine whether different predators target distinct microorganisms, how interactions among protozoans affect resource (microorganism) use, and how predator diversity affects prey community diversity. In particular, we endeavored to determine if protozoa followed known ecological patterns such as keystone predation or generalist predation. For these experiments, replicate inquiline microbial communities were maintained for seven days with five protozoan species. Microbial community structure was determined by 16S rRNA gene amplicon sequencing (iTag) and analysis. Compared to the control (no protozoa), two ciliates followed patterns of keystone predation by increasing microbial evenness. In pairwise competition treatments with a generalist flagellate, prey communities resembled the microbial communities of the respective keystone predator in monoculture. The relative abundance of the most common bacterial Operational Taxonomic Unit (OTU) in our system decreased compared to the control in the presence of these ciliates. This OTU was 98% similar to a known chitin degrader and nitrate reducer, important functions for the microbial community and the plant host. Collectively, the data demonstrated that predator identity had a greater effect on prey diversity and composition than overall predator diversity.

Diverse microbial communities hosted by the model carnivorous pitcher plant Sarracenia purpurea: analysis of both bacterial and eukaryotic composition across distinct host plant populations

“…The dominance of Proteobacteria and Bacteriodetes in pitchers in both wetlands is similar to our preliminary genetic screening of these populations (Young, Sielicki & Grothjan, 2018) and to previous studies of pitcher plant bacterial communities, where α , β and γ -Proteobacteria were dominant and Bacteroidetes and Firmicutes were common (Peterson et al, 2008; Koopman et al, 2010; Gray et al, 2012; Armitage, 2017; Canter et al, 2018). Bacterial classes were the same as those typically found in wetland soils (Zhang et al, 2017).…”

“…However, the most common phylum, Saccharibacteria AT (formerly TM7), is known in wetlands, soil and aquatic habitats (Hugenholtz et al, 2001), but has previously been reported only in very low abundance in pitcher plants (Morales et al, 2006; Krieger & Kourtev, 2012). The common families Sphingomonodaceae, Rhodospirillaceae, Oxalobacteraceae and many of the most abundant genera ( Pedobacter , Aquitalea, Sphingomonas, Rickettsiella , Azospirillum ) are common with previous reports for pitcher communities (Gray et al, 2012; Northrop et al, 2017; Canter et al, 2018; Young, Sielicki & Grothjan, 2018).…”

“…Bactivorous protozoa including flagellates and ciliates are well-documented within S. purpurea (Hegner, 1926; TerHorst, 2011; Miller & Kneitel, 2005; Miller & TerHorst, 2012). Dominance of Colpoda species, which were found in both wetlands, and Tetrahymena sp., which was only found in Sapa, has also been reported in pitcher plants (Rojo-Herguedas & Olmo, 1999; TerHorst, 2011) and dominant ciliates are known to influence community composition (Paisie, Miller & Mason, 2014; Canter et al, 2018). The large diversity of ciliates encountered could be related to low abundance or absence in some pitchers of mosquito larvae taxa (including W. smithii ), which typically predate ciliates and other protozoa in pitchers; CB1p4 had the highest ciliate sequence count and lacked all mosquito taxa.…”

“…Colonization of more diverse bacterial communities was also not dependent on more diverse eukaryotic representation, as Sapa samples showed higher eukaryotic diversity but lower bacterial diversity than Cedarburg samples. Early studies assumed that the largest source of bacteria within pitchers is transferred from prey (Hepburn & St John, 1927), and there is good experimental evidence that presence of invertebrate or protist taxa influences bacterial composition (Peterson et al, 2008; Paisie, Miller & Mason, 2014; Canter et al, 2018). However, contributions of bacterial taxa from prey versus wind, rain or other non-prey sources needs to be more rigorously examined.…”

Disparities in the analysis of morphological disparity

“…Thankfully, this is becoming easier through the availability of diverse, welldocumented R packages for multidimensional analysis [42,[65][66][67][68]. Many of the methods employed in disparity analysis are used more widely in other fields, including genomics and ecology, which also encompass analyses of multidimensional datasets [69][70][71][72]. Innovations in morphological disparity analyses likely await discovery in their respective literatures.…”