Bacteria dispersal by hitchhiking on zooplankton

Abstract

Microorganisms and zooplankton are both important components of aquatic food webs. Although both inhabit the same environment, they are often regarded as separate functional units that are indirectly connected through nutrient cycling and trophic cascade. However, research on pathogenic and nonpathogenic bacteria has shown that direct association with zooplankton has significant influences on the bacteria's physiology and ecology. We used stratified migration columns to study vertical dispersal of hitchhiking bacteria through migrating zooplankton across a density gradient that was otherwise impenetrable for bacteria in both upward and downward directions (conveyor-belt hypothesis). The strength of our experiments is to permit quantitative estimation of transport and release of associated bacteria: vertical migration of Daphnia magna yielded an average dispersal rate of 1.3 x 10(5) x cells x Daphnia(-1) x migration cycle(-1) for the lake bacterium Brevundimonas sp. Bidirectional vertical dispersal by migrating D. magna was also shown for two other bacterial species, albeit at lower rates. The prediction that diurnally migrating zooplankton acquire different attached bacterial communities from hypolimnion and epilimnion between day and night was subsequently confirmed in our field study. In mesotrophic Lake Nehmitz, D. hyalina showed pronounced diel vertical migration along with significant diurnal changes in attached bacterial community composition. These results confirm that hitchhiking on migrating animals can be an important mechanism for rapidly relocating microorganisms, including pathogens, allowing them to access otherwise inaccessible resources.

Fig. 1.

Transport and dispersal of bacteria in the water column. Free bacteria (1) may attach to suspended matters such as microgels (2) and particles (3) that form large sinking aggregates (4) and transport the bacteria to deeper water. Free bacteria may also be ingested by grazers and subsequently, released as part of the fecal matter (5), which also helps transport the bacteria to deeper water. These mechanisms work primarily in the downward direction. Alternatively, free bacteria may attach to large and motile organisms (6), which, through horizontal and vertical migration, transport the bacteria across aquatic boundary layers, such as thermo-, chemo-, and pycnoclines, that are otherwise impassable for the bacteria. Unlike passively sinking aggregates, large motile organisms can cover long distances in a short time and transport bacteria in both downward and upward directions. As such, migrating organisms function as a conveyor belt within the water column to facilitate the dispersal and exchanges of bacteria between isolated water masses.

Fig. 2.

Upward (Left) and downward (Right) transport of Brevundimonas sp. in migration columns with different numbers of D. magna (● = 0; ▼ = 20; ■ = 80). D. magna completed one migration cycle (downward + upward) across the pycnocline every 2 h. Error bars represent SEs of 10 bacterial counts. Numbers next to lines are slopes of linear regressions (P < 0.05). NS, not significant. Full statistics are provided in Table S1.

Fig. 3.

(A) Water-temperature profile for Lake Nehmitz and relative vertical distribution of D. hyalina at midday and midnight. (B) Cluster analysis of DGGE banding patterns of bacterial communities on D. hyalina collected at different depths and times of the day. (C) ANOSIM analysis testing for differences in bacterial community composition on D. hyalina collected at different depths and time (details in Text).