where are we by now .fr

Flagellate bacterivory and viral lysis are now known to be two major sources of bacterial mortality: Dozens of papers have been published individually. Viral lysis ...
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RELATIONSHIPS BETWEEN VIRUSES, BACTERIA AND PROTOZOAN GRAZERS IN AQUATIC ENVIRONMENTS:

WHERE ARE WE BY NOW ?

S Jacquet 1, K Simek 2, M Weinbauer 3, T Sime-N’Gando 4, T Bouvier 5, Y Bettarel 6

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1. UMR CARRTEL, INRA, Group of Aquatic Microbial Ecology, Thonon-les-Bains, France 2. Hydrobiological Institute, Czechoslovak Academy of Sciences, Ceske Budejovice, Czechoslovakia 3. LOV, Microbial Ecology and Biogeochemistry Group, Villefranche-sur-Mer, France 4. Laboratoire de Biologie des Protistes, Université Blaise Pascal, Aubière, France 5. Equipe d’Ecologie Bactérienne des Milieux Aquatiques côtiers, Université de Montpellier 2, Montpellier, France 6. Centre IRD de Bel-Air, Dakar, Senegal

OUTLINE LET’S GO TO THE THEATRE

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INTRODUCTION

The characters ?

ACT 1, 2 scenes

HNF and viruses, main predators of bacteria ?

ACT 2, 1 scene

HNF, predators of viruses ?

ACT 3, 1 scene

HNF, preys of viruses ?

ACT 4, 1 scene?

Bacteria, killers of viruses ?

ACT 5, 1 scenes?

Bacteria, killers of bacteria ?

ACT 6, 1 scene?

VIBM stimulated by grazers ?

EPILOGUE

What is still missing ? So many questions yet ! Possible ‘take home messages’ ? Redrawing aquatic microbial food webs ?

THE CHARACTERS WHO WILL BE ON STAGE TODAY ?

C F

B V

In :

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” TO LIVE AND LET DIE ”

HNF GRAZERS STATE OF THE ART, SCIENTIFIC INTEREST, POTENTIAL ROLE

Affect bacterial diversity

Modify bacterial traits

Size reduction Filament formation Floc formation Biofilm formation

Modify bacterial physiology Secondary metabolites prod Expolymer formation

Decline and control of bacterial blooms

High speed motility Toxin release BP ↑

Food for other protists Microbial mortality 4/30

Recycling Biogeochemistry

Inductor of aggregates

VIRUSES STATE OF THE ART, SCIENTIFIC INTEREST, POTENTIAL ROLE

Microbial diversity

Production of toxins Lysogeny)) (Lysogeny

Genetic recombination

(Killing the winner ?)

DMS formation

Decline and control of algal blooms

Microbial mortality 5/30

(Killing the winner ?)

Food for protists

Recycling Biogeochemistry

Inductor of aggregates

ACT 1 : HNF GRAZERS AND VIRUSES, MAIN PREDATORS OF BACTERIA ?

Viral attack of bacteria

HNF grazing bacteria

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ACT 1 : HNF GRAZERS AND VIRUSES, MAIN PREDATORS OF BACTERIA ? Flagellate bacterivory and viral lysis are now known to be two major sources of bacterial mortality: Dozens of papers have been published individually Viral lysis is responsible for 5-50% (up to 90%) of daily bacterial mortality HNF grazing is responsible for 5-250% of daily bacterial mortality However, only a few studies have compared simultaneously VIBM vs. protistan grazing: 14 published papers from the first direct comparisons of losses attributable to viruses and protists by Bratbak et al (1992) followed by Fuhrman & Noble (1995) and Weinbauer & Peduzzi (1995) using different approaches Only 1 for the benthal (published in 2006 by Fischer et al) ! Only 1 considering a long time series (published in 2005 by Pradeep Ram et al) ! From Pradeep Ram et al (2005) ME

Virus-induced bacterial lysis

ACT 1 : HNF GRAZERS AND VIRUSES, MAIN PREDATORS OF BACTERIA ? On average phage-mediated mortality of bacterioplankton is as high as grazing mediated mortality. These two factors/processes of bacterial mortality do not always balance daily bacterial production However, their relative contribution change strongly with time, space and systems Viral lysis > Grazing : when high abundance of bacteria, low BSR or ‘special’ conditions are met (in deep ocean or lakes, with increasing anoxy, in cold waters, in hypersaline waters) Bacterial mortality

shift

From Weinbauer & Hofle (1998) AEM

From Colombet et al. (2006) AEM

ACT 1 : HNF GRAZERS AND VIRUSES, MAIN PREDATORS OF BACTERIA ?

But not always ! Viral lysis > Grazing in ‘normal’ conditions (ex: Oxbow lake of the Danube River, Lake Bourget) ! Somehow, trophic status dependent This viral shunt has still to be studied in more details since it may considerably reduce the significance of the bacteria-flagellate link

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HNF-induced bacterial mortality

ACT 2 : HNF GRAZERS, PREDATORS OF VIRUSES ? HNF eating a virus

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ACT 2 : HNF GRAZERS, PREDATORS OF VIRUSES ? Virivory : omnivory (grazing of free living particles) or coincidental (grazing on infcells) 1st suggestion by Suttle & Chen (1992) 1st demonstration by Gonzales & Suttle (1993) A possible relationship from HNF-virus correlations in Weinbauer & Peduzzi (1995) The model of Binder (1999) for VIBM estimation takes into account grazing of infected cells at the same rate than uninfected cells 1st suggestions & evidences in freshwaters (Manage et al 2000 & 2002) 2nd important demonstration in freshwaters (Bettarel et al 2005) with a long term study (April to November) for two lakes with contrasting trophic status 1 model dealing with intraguild predation (Miki & Yamamura 2005) : omnivory vs. coincidental IGP

From Manage et al. (2002) Ecol Res

From Bettarel et al. (2005) AME

ACT 2 : HNF GRAZERS, PREDATORS OF VIRUSES ? Phagotrophy by nanoflagellates seems to be of minor importance as a loss process for natural virioplankton communities The transfer of carbon to the higher trophic levels via this activity seems to be of minor importance (pelagial and benthal) Besides, the CPN represent only a small fraction of diet compared to bacteria (> 50 M = 4.1% VP: oligo M = 0.8% VP : eutro

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Possibility of the presence of specialist grazers on viruses in low productive systems and in the sediments

3

Whatever the importance of such a link between viruses and HNF, it exists and may vary greatly with time, space and ecosystem. Q: Possible consequences on bacterial dynamics and diversity ?

2 1 0 E

M

H

From Bettarel et al. (2005) AME

ACT 2 : HNF GRAZERS, PREDATORS OF VIRUSES ? The model dealing with intraguild predation (Miki & Yamamura 2005): “kill the killer of the winner (KKW)” The model suggests that : - grazing of flagellates on infected cells may yield a decrease in bacterial species richness since the KKW reduces the VBR, which undermises the KW process - the KKW process is influenced by the latent period: the highest, the lowest BSR (by causing the viruses in hosts to be more at risk of being killed by grazing) Coincidental IGP

in consequence : HNF – virus interactions still have to be studied in more details

Coincidental IGP

ACT 3 : HNF GRAZERS, PREYS OF VIRUSES ?

Virus infecting HNF

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ACT 3 : HNF GRAZERS, PREYS OF VIRUSES ?

Following Suttle & Chen (1992) who were the first to report that flagellates are capable of ingesting and digesting viruses, a question emerged Q: To what extent does viral ingestion represent a source of infection for the HNF? Note that this question was again asked in the conclusion of Bettarel et al (2005) Only 1 paper reporting the isolation and characterization of a dsDNA virus infecting a HNF (Bodo sp) by Garza & Suttle (1995) Some suggestions elsewhere but never investigated I think ! Still, the mechanism of infection by these viruses is unknown so that it is not clear whether grazing on viral particles affects the probability that the flagellates will be infected

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ACT 4 : BACTERIA, KILLERS OF VIRUSES ?

Bacterial defense against viruses

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ACT 4 : BACTERIA, KILLERS OF VIRUSES ?

Degradation or digestion of viruses by bacterial exoenzymes Bacterial resistance to viral attack These processes can be considered as other KKW processes since bacterial cells ‘kill’ themselves viruses, leading to lower BSR Bacterial defense against viruses

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ACT 5 : INTERACTIONS OF BACTERIA WITH OTHER BACTERIA ?

Bacterial predator of bacteria

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ACT 5 : INTERACTIONS OF BACTERIA WITH OTHER BACTERIA ? Bdellovibiro and BALO like organisms : unmasked and now seen predator Ubiquitous Generally in low concentrations but sometimes (thousands of cells) Specific of gram – bacteria It is likely that these predators, even if they are not dominant populations, may contribute significantly to bacterial mortality in aquatic ecosystems Nothing is known on that as well as viral impact and grazing by HNF or other eukaryotic grazers on these bacterial predators !

What about virus-virus interactions ? (Neutralism, Competition, Mutualism, Commensalism, Amensalism) But these are not really feeding relationships !

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ACT 6 : SYNERGISTIC RELATIONSHIPS BETWEEN VIRUSES AND HNF ?

Synergistic relationships between viruses and HNF

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ACT 6 : SYNERGISTIC RELATIONSHIPS BETWEEN VIRUSES AND HNF ?

Because phages and flagellates consume the same prey, an antagonistic interaction may be expected, i.e. an increase in the activity of one type of consumer could result in a decrease in "resources" for the other consumer of bacteria. This indicates more a competition than a coupling between grazers and viruses for prey However…

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ACT 6 : SYNERGISTIC RELATIONSHIPS BETWEEN VIRUSES AND HNF ? Simek and co-authors were the first in 2001 to report that protistan grazing may stimulate (increase) viral lysis suggesting a synergy between grazing and virus-induced mortality in a meso-eutrophic reservoir (Rimov, CR) Since this study, such a synergy has been reported elsewhere : 2 other published papers : Weinbauer et al (2003) - Rimov reservoir, Sime-NGando & Pradeep (2005) - Massif Central Lakes At least, 4 unpublished yet (in French Alpine Lakes, W Med Sea, Rimov reservoir ) But also 5 papers in which such a synergy was not observed or confirmed : Marranger et al (2002), Bettarel et al (2004), Hornak et al (2005), Jardillier et al (2005), Bongiorni et al (2005), sometimes in the same ecosystem than mentioned above !

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Bacterial abundance 6 -1 (10 cells ml ) Frequency of visibly infected bacteria (%)

50 40 30 20 10

0

24 48 72 Time (hours)

96

35 30

Grazing3 enhanced treatment (< 5 µm)

25 20

2

15

Lowest bacterial abundance 1 Highest 0 viral 24abundance 48 72

FRACTIONATION

10 96

Highest virus -induced Time (hours) bacterial mortality rates

0

24

48

72

96

Bacterail mortality due to viral lysis (%)

4

Reservoir < 5 µm < 0.8 µm

Viral abundance 6 -1 (10 ml )

14 12 10 8 6 4 2 0

Time (hours) From Simek al (2001) AEM

ACT 6 : SYNERGISTIC RELATIONSHIPS BETWEEN VIRUSES AND HNF ?

From Sime-N’Gando & Pradeep Ram (2005) AME

ACT 6 : SYNERGISTIC RELATIONSHIPS BETWEEN VIRUSES AND HNF ? 18

A Exp B1

Lake Bourget, French Alpine Lake, surface, 3 periods, mesotrophic

12

VIBM (%)

6

Community size fractionation 0 < 1.2

9