Synergistic and antagonistic effects of viral lysis and protistan grazing on bacterial biomass, production and diversity

Abstract

In a mesotrophic reservoir, we examined the effects on the bacterioplankton of distinct consumers of bacteria, viruses and heterotrophic nanoflagellates, both alone and combined in an experiment using natural populations and in situ incubations in dialysis bags. Ribosomal RNA-targeted probes were employed as well as 16S RNA gene based PCR denaturing gradient gel electrophoresis (DGGE) to enumerate bacterial groups and assess bacterial community composition. We employed probes for Actinobacteria (HGC69a probe), Cytophaga-Flavobacterium-Bacteroidetes bacteria (CF319a probe), BET42a probe (Betaproteobacteria) and a subgroup-Betaproteobacteria (R-BT065 probe). We found consumer-specific effects on bacterial activity and diversity (against a background of CF and BET dominating all treatments) suggesting distinct vulnerabilities to the two sources of mortality. For example, growth rate of Actinobacteria was only positive in the presence of flagellates, while towards the end of the experiment (T(72-96 h)) growth rate of R-BT was only positive in the viruses only treatment. More specific data on how viruses and flagellates influenced Flectobacillus are shown in the companion paper. Highest richness (number of DGGE bands) was found in the virus only treatment and lowest when both consumers were present. In addition, we found suggestions of both antagonistic and synergistic interactions between the two sources of bacterial mortality. Notably, bactivory by flagellates was associated with reductions in bacterial diversity and increases in viral production.

Trade-Offs between Competition and Defense Specialists among Unicellular Planktonic Organisms: the “Killing the Winner” Hypothesis Revisited

“…Filamentous prokaryotic forms appeared in both treatments but were twice as abundant, long, and active in incubations with both predators than in the flagellate treatment alone. In a companion paper, Weinbauer et al (103) found that the vulnerability to the two sources of mortality (viruses and flagellates) was distinctly different between prokaryotic groups (see also reference 38). However, in contradiction to KtW (Fig.…”

Indirect interactions in the microbial world: specificities and similarities to plant–insect systems

“…For example, from the point of TMII theory, viruses can potentially be the initiator that induces trait changes in bacteria, and in turn, HNF can be the receiver of induced trait changes, as it has also been suggested that viral infections affect bacterial growth and composition through a variety of processes, including nutrient regeneration, host-specific infection, occurrence of some resistant types, and killing the winner or looser (Thingstad and Lignell 1997;Fuhrman 1999;Thingstad 2000;Bouvier and del Giorgio 2007;Š imek et al 2007;Suttle 2007;. However, to the best of our knowledge, there are no reports suggesting positive or negative indirect effects of viruses on HNF Weinbauer et al 2007;Zhang et al 2007). Therefore, it would be unlikely that viral-lysis-induced changes in bacterial assemblage can contribute to the coexistence of HNF and viruses.…”

“…The combined effects of shortterm physiological responses of bacteria and viruses and their coevolutionary outcomes make it difficult to predict the general patterns of the impact of system productivity on the viral contribution to bacterial mortality. Enhanced bacterial growth and induced bacterial trait changes could also explain the many experimental findings showing that the presence of HNF, i.e., the trophic interaction between HNF and bacteria, leads to an increase in viral production rate, frequency of infected bacterial cells, and viral abundance Weinbauer et al 2003Weinbauer et al , 2007Sime-Ngando and Pradeep Ram 2005;Jacquet et al 2007;Pradeep Ram and Sime-Ngando 2008). Although HNF have lethal effects on individual bacteria, HNF predation is known to stimulate the growth rate of the surviving individuals, i.e., both the biomass growth rate and the replication rate, by changing the resource conditions and weakening competition for resources.…”

“…1c). This scenario is essential to understand the synergistic effects between HNF and viruses Weinbauer et al 2003Weinbauer et al , 2007Sime-Ngando and Pradeep Ram 2005). Interestingly, however, several studies in similar experimental settings have also shown that HNF predation can reduce viral activity and abundance (Maranger et al 2002;Bongiorni et al 2005;Horňák et al 2005;Jardillier et al 2005).…”

The importance of protozoan bacterivory in a subtropical environment (Lobo-Broa Reservoir, SP, Brazil)

“…Pinhassi et al, 2006), predation (e.g. Weinbauer et al, 2007), viral lysis (e.g. Motegi et al, 2009) and temperature (e.g.…”