Microbial Food Webs in Boreal Humic Lakes and Reservoirs: Ciliates as a Major Factor Related to the Dynamics of the Most Active Bacteria

Abstract

In order to assess the factors that determine the dynamics of bacteria with high nucleic acid content in aquatic systems, we (i) conducted 24-h in situ dialysis experiments, involving different fractions of plankton and unfiltered water and (ii) examined empirical relationships between bacteria and both abiotic factors and protists, in boreal humic freshwaters (reservoir and lakes) in the James Bay region (Québec, Canada). Bacteria were subdivided into two subgroups on the basis of their nucleic acid content assessed by flow cytometry. The abundance of bacteria with the highest nucleic acid content and high light scatter (HNA-hs) was significantly correlated, across sites, to bacterial production, whereas bacteria with lower nucleic acid content (LNA) and total bacteria were not. In addition, HNA-hs growth was higher and more variable than LNA growth, indicating that HNA-hs were the most dynamic bacteria. Heterotrophic nanoflagellate and ciliate biomass represented, on average, 5 and 13% of bacterial biomass, respectively. Both in ambient waters and in experiments, ciliates were significantly and negatively correlated with bacteria, whereas heterotrophic nanoflagellates, likely under the grazing pressure from ciliates and metazooplankton, were not. Among ciliates, Cyclidium glaucoma appeared to play an important role. Its growth was significantly and negatively correlated to that of HNA-hs but not to that of LNA. In ambient waters, the abundance of this species explained 56% of the variations in HNA-hs abundance and only 27% of those for LNA. The abundances of total bacteria and LNA significantly increased with chlorophyll a, whereas those of HNA-hs did not. In addition, during the experiments, the estimated potential losses of HNA-hs significantly increased with the initial abundance of C. glaucoma. These results suggest selective removal of the most dynamic bacteria by C. glaucoma and indicate that ciliates may play an important role in the dynamics of active bacteria in natural waters. These findings suggest the existence, within the aquatic microbial food webs, of keystone species that are very important in regulating the activity structure of bacteria.

Assessing the relevance of nucleic acid content as an indicator of marine bacterial activity

“…LNA cell abundance did not increase with increasing chl a or bacterial activity, as previously observed in natural samples (Morán et al 2002b, Tadonléké et al 2005 and in dilution-growth experiments (Gasol et al 1999, Vaqué et al 2001, altogether supporting their identification with inactive or dead cells, as proposed by some authors (Li et al 1995, Jellett et al 1996, Gasol et al 1999. However, the finding that overall LNA bacterial abundance was more variable than that of HNA cells (76 vs. 62% CV; see also Table 1), if not an indirect result of factors acting on HNA bacteria, could suggest that this group of cells was able to show some response to environmental forcing (Seymour et al 2005, Sherr et al 2006).…”

“…5). In a recent paper, Tadonléké et al (2005) concluded that grazing by ciliates was a major factor responsible for lack of response of HNA abundance to chl a in a series of lakes. Although mortality by protistan grazers or viral infection was not assessed during the present study, the lower biomass of HNA cells in the East zone could be indicative of a preferential loss of the most active and larger cells within this group.…”

Marine bacterial community structure resilience to changes in protist predation under phytoplankton bloom conditions

“…The physiological state of bacterial cells has also been suggested as a key factor in grazing selectivity (Del Giorgio and Gasol, 2008), and preferential grazing of the more active cells within a community by protist grazers has been repeatedly observed (Del Giorgio et al, 1996;Pernthaler et al, 1997;Simek et al, 1997;Tadonléké et al, 2005;Sintes and Del Giorgio, 2014). This is probably related to the general positive relation between cell size and activity in marine bacteria (Gasol et al, 1995;Hahn and Höfle, 2001;Matz and Jürgens, 2001;Matz et al, 2002;Corno and Jürgens, 2006), suggesting that larger bacterioplankton cells are also usually the most active ones.…”

Geographic distribution pattern of low and high nucleic acid content bacteria on a river-catchment scale

“…It has been shown that heterotrophic nanoflagellates and other planktonic predators seem to prefer grazing on and selectively cropping the largersized and more active fraction of bacterioplankton (Corzo et al 2005;Nishimura et al 2005). Tadonleke and co-workers reported that Cyclidium glaucoma selectively grazed on HNA communities rather than on LNA (Tadonléké et al 2005). Nishimura and colleagues also found that the grazing mortality of HNA bacteria was 2.8-fold higher than that of LNA bacteria in Lake Biwa (Nishimura et al 2005).…”