Abstract
Protistan bacterivory, a microbial process involving ingestion and digestion, is ecologically important in the microbial loop in aquatic and terrestrial ecosystems. While bacterial resistance to protistan ingestion has been relatively well understood, little is known about protistan digestion in which some ingested bacteria could not be digested in cells of major protistan grazers in the natural environment. Here we report the phylogenetic identities of digestion-resistant bacteria (DRB) that could survive starvation and form relatively stable associations with 11 marine and one freshwater ciliate species. Using clone library and sequencing of 16S rRNA genes, we found that the protistan predators could host a high diversity of DRB, most of which represented novel bacterial taxa that have not been cultivated. The localization inside host cells, quantity, and viability of these bacteria were checked using fluorescence in situ hybridization. The DRB were affiliated with Actinobacteria, Bacteroidetes, Firmicutes, Parcubacteria (OD1), Planctomycetes, and Proteobacteria, with Gammaproteobacteria and Alphaproteobacteria being the most frequently occurring classes. The dominance of Gamma- and Alphaproteobacteria corresponds well to a previous study of Global Ocean Sampling metagenomic data showing the widespread types of bacterial type VI and IV secretion systems (T6SS and T4SS) in these two taxa, suggesting a putatively significant role of secretion systems in promoting marine protist-bacteria associations. In the DRB assemblages, opportunistic bacteria such as Alteromonadaceae, Pseudoalteromonadaceae, and Vibrionaceae often presented with high proportions, indicating these bacteria could evade protistan grazing thus persist and accumulate in the community, which, however, contrasts with their well-known rarity in nature. This begs the question whether viral lysis is significant in killing these indigestible bacteria in microbial communities. Taken together, our study on the identity of DRB sheds new light on microbial interactions and generates further hypotheses including the potential importance of bacterial protein secretion systems in structuring bacterial community composition and functioning of “microbial black box” in aquatic environments.
Highlights
Protistan grazing on bacteria is one of the most important ecological processes in microbial food webs that channel carbon and energy to higher trophic levels and regenerate nutrients (Azam et al, 1983)
Classification via ribosomal database project (RDP) classifier pipeline showed that the digestion-resistant bacteria (DRB) were highly diverse
Effective protistan grazing on bacteria relies on the success of two successive steps, ingestion and digestion, of which the latter has been rarely studied for nanoflagellates and ciliates from an ecological perspective
Summary
Protistan grazing on bacteria is one of the most important ecological processes in microbial food webs that channel carbon and energy to higher trophic levels and regenerate nutrients (Azam et al, 1983). In the long evolutionary history of the interplay between bacterial preys and protistan predators, bacteria have seemingly developed many strategies to survive protistan grazing These include: changes in cell size and filamentation, formation of aggregates, microcolonies and biofilms, increases of swimming speed, and chemical resistance to ingestion (for reviews see Jürgens and Güde, 1994; Hahn and Höfle, 2001; Jürgens and Matz, 2002; Matz and Kjelleberg, 2005; Pernthaler, 2005; Montagnes et al, 2008). Many bacterial strains (e.g., Legionella, Listeria, Vibrio, and Salmonella) could persist inside Acantbamoeba and Tetrahymena cells, which might have given rise to intracellular symbionts, parasites, and pathogens (Barker and Brown, 1994; Greub and Raoult, 2004; Brandl et al, 2005; Matz and Kjelleberg, 2005). What has not been investigated much, so far, is the diversity and composition of the bacterial assemblages that are resistant to digestion by major protistan bacterivores in complicated microbial communities of aquatic systems
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