Betaproteobacteria Limnohabitans strains increase fecundity in the crustacean Daphnia magna: symbiotic relationship between major bacterioplankton and zooplankton in freshwater ecosystem

Abstract

How symbioses between bacteria and aquatic animals influence food webs in freshwater ecosystems is a fundamental question in ecology. We investigated symbiosis between a crustacean zooplankton Daphnia magna and its dominant bacterial symbiont Limnohabitans, an abundant and globally distributed freshwater Betaproteobacteria. Aposymbiotic juvenile Daphnia were prepared and exposed to any of four Limnohabitans sp. - Limnohabitans strains DM1, 2KL-3, 2KL-7 and Limnohabitans planktonicus strain II-D5, all previously found in D. magna digestive tract or culture. Re-infected Daphnia were cultured until they produced the first clutch of juveniles. Limnohabitans strain DM1 and L. planktonicus strain II-D5 successfully re-infected Daphnia through single exposure at the first instar juvenile stage. In contrast to aposymbiotic Daphnia that produced non-viable juveniles, re-infected Daphnia produced viable juveniles and increased fecundity to levels of that of symbiotic Daphnia. Re-infected Daphnia did not increase their number of eggs nor growth rates. Limnohabitans strains 2KL-7 and 2KL-3 could not recover fecundity even in multiple exposures during culture. This study shows the functional evidence demonstrating that a single bacterium Limnohabitans regulates fecundity of the consumer Daphnia through symbiosis. Our results indicated that symbiotic relationship between major bacterioplankton and zooplankton is important for maintaining the population of zooplankton in freshwater ecosystems.

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

“…showed that inoculating germ-free Daphnia with these bacteria had a positive effect on host fitness, although for Limnohabitans sp. this was found to be restricted to specific strains (Sison-Mangus et al, 2014;Peerakietkhajorn et al, 2015b). Interestingly, the dominant Aeromonas sp.…”

Life history and eco‐evolutionary dynamics in light of the gut microbiota

“…In all these species, inoculating axenic larvae with gut bacteria can restore a normal developmental rate (Storelli et al 2011, Coon et al 2014, Callens et al 2016. Mono-association studies in Drosophila (Shin et al 2011, Storelli et al 2011), mosquitoes (Coon et al 2014) and Daphnia (Peerakietkhajorn et al 2016) further identified single bacterial strains that are sufficient to recapitulate the natural microbiota growth-promoting effect. In Drosophila, these bacteria exert their beneficial functions on the host by promoting insulin signaling (Shin et al 2011, Storelli et al 2011.…”

Temperature-dependent benefits of bacterial exposure in embryonic development of Daphnia magna resting eggs

“…The beneficial role of bacteria could be related to specific characteristics of resting eggs, such as the tertiary membrane. However, one study reported high rates of inviability and developmental abnormalities in the parthenogenetic eggs of microbiota-free Daphnia mothers under sterile conditions (Peerakietkhajorn et al, 2015). As gut microbiota are thought to contribute to the nutrition of adult Daphnia (Gorokhova et al, 2015), and resting eggs are often produced under conditions of high crowding that are accompanied by food scarcity, sensitivity to the absence of bacteria could be a characteristic of eggs produced by undernourished mothers.…”

“…At this stage, the asexual eggs are still encased in a chorion, similar to diapausing eggs. The collected eggs were surface-sterilized following the protocol of Peerakietkhajorn et al (2015). In short, the eggs were incubated for 30 min in 0.25% glutaraldehyde and washed three times with sterile water before they were placed individually in the wells of a 96-well plate.…”