Bacterial epibionts of Daphnia: a potential route for the transfer of dissolved organic carbon in freshwater food webs

Abstract

The identification of interacting species and elucidation of their mode of interaction may be crucial to understand ecosystem-level processes. We analysed the activity and identity of bacterial epibionts in cultures of Daphnia galeata and of natural daphnid populations. Epibiotic bacteria incorporated considerable amounts of dissolved organic carbon (DOC), as estimated via uptake of tritiated leucine: three times more tracer was consumed by microbes on a single Daphnia than in 1 ml of lake water. However, there was virtually no incorporation if daphnids were anaesthetised, suggesting that their filtration activity was essential for this process. Microbial DOC uptake could predominantly be assigned to microbes that were located on the filter combs of daphnids, where the passage of water would ensure a continuously high DOC supply. Most of these bacteria were Betaproteobacteria from the genus Limnohabitans. Specifically, we identified a monophyletic cluster harbouring Limnohabitans planktonicus that encompassed sequence types from D. galeata cultures, from the gut of Daphnia magna and from daphnids of Lake Zurich. Our results suggest that the epibiotic growth of bacteria related to Limnohabitans on Daphnia spp. may be a widespread and rather common phenomenon. Moreover, most of the observed DOC flux to Daphnia in fact does not seem to be associated with the crustacean biomass itself but with its epibiotic microflora. The unexplored physical association of daphnids with heterotrophic bacteria may have considerable implications for our understanding of carbon transfer in freshwater food webs, that is, a trophic 'shortcut' between microbial DOC uptake and predation by fish.

Food availability affects the strength of mutualistic host–microbiota interactions in Daphnia magna

“…to be the dominant taxon, this is in accordance with earlier studies who also found this taxon to be a major constituent of the Daphnia microbiota (Freese & Schink, 2011;Eckert & Pernthaler, 2014;Gorokhova et al, 2015). However, by specifically characterizing the gut microbiota, we found that in our cultures Aeromonas sp.…”

“…Daphnia is known to harbor high numbers of bacteria on the surface of its body and in its gut (Grossart et al, 2010;Eckert & Pernthaler, 2014), and Qi et al (2009) showed that several bacterial taxa are consistently found in affiliation with Daphnia, even in geographically separated populations, indicating a highly specific association between Daphnia and its microbiota. Notably, the β-proteobacterial genus Limnohabitans (Comamonadaceae) seems to be a major constituent of the Daphnia microbiota (Freese & Schink, 2011;Eckert & Pernthaler, 2014;. Sison-Mangus et al (2014) showed, by comparing bacteria-free Daphnia with conventional ones, that the relationship between D. magna and its microbiota is mutualistic, as removing the microbiota results in decreased growth, survival and reproduction of the host.…”

“…D. magna is a keystone species in many freshwater habitats and has been widely used as an experimental system to study ecological and evolutionary interactions (for example, Decaestecker et al, 2007;Miner et al, 2012). Daphnia is known to harbor high numbers of bacteria on the surface of its body and in its gut (Grossart et al, 2010;Eckert & Pernthaler, 2014), and Qi et al (2009) showed that several bacterial taxa are consistently found in affiliation with Daphnia, even in geographically separated populations, indicating a highly specific association between Daphnia and its microbiota. Notably, the β-proteobacterial genus Limnohabitans (Comamonadaceae) seems to be a major constituent of the Daphnia microbiota (Freese & Schink, 2011;Eckert & Pernthaler, 2014;.…”

Competition and niche separation of pelagic bacteria in freshwater habitats

“…This ‘hitch hiking’ provides bacteria with a means of increasing their dispersal (Grossart et al ., ), and, in turn, is also beneficial to their hosts (Sison‐Mangus et al ., ; Peerakietkhajorn et al ., ). Moreover, the consumption of zooplankton together with their attached microflora by fish may represent a shortcut within microbial food webs that increases DOC transfer efficiency by several orders of magnitude (Eckert and Pernthaler, ).…”

Prey-Specific Growth Responses of Freshwater Flagellate Communities Induced by Morphologically Distinct Bacteria from the Genus Limnohabitans

“…Limnohabitans bacteria from the R-BT cluster are omnipresent in a wide variety of pHneutral or alkaline freshwater habitats (16). However, they have been also found as microflora in the digestive tract of algivorous Daphnia magna (22) or as epibionts in filter combs of Daphia galeata (23). Thus, it seems that the main substrates supporting their rapid growth in situ are alga-derived substances (19,24,25).…”