Viruses : Conductors of aquatic ecosystems ? Stéphan JACQUET Thonon-les-Bains

Outline ¾ The Group of Aquatic Microbial Ecology ¾ The Importance of Aquatic Ecosystems ¾ The Importance of Aquatic Micro-organisms ¾ The Importance of Aquatic Viruses ¾ The Key Roles played by Aquatic Viruses ¾ The Uncharacterized Viral Diversity ¾ The Phage Therapy in Aquatic Environments ¾ Take Home Messages

GAME Group of Aquatic Microbial Ecology

Evaluate and study the diversity, the dynamics and the functioning of aquatic microbial communities, from viruses to protozoan

The French Aquatic Viral Network

AQUAPHAGE

Relationships between prokaryotic and viral diversity in different aquatic environments

Genomics & Ecology of Aquatic Viruses Banyuls-sur-Mer, France 11-13 February, 2008

A meeting in the context of the Marine Genomics Europe Network and

RAVAGE Réseau frAnçais de Virologie Aquatique de la Génomique à l'Ecologie

Aquatic Ecosystems

ƒ Aquatic habitats represent >70% of the Earth’ surface ƒ >50% of the ocean is >3,000 m depth (V=1.3 x 109 km3) ƒ Freshwater ecosystems represent 0.02% of the total water volume ƒ The oceans control the climate, produce half of the Earth’s oxygen

Aquatic Microorganisms ƒ Microorganisms constitute >90% of living biomass in the sea ƒ Prokaryotes dominate over unicellular eukaryotes by a factor of 2-3 orders of magnitude in the pelagic environment ƒ Total number of prokaryotes in aquatic habitats : 1.2 x 1029 cells ~ similar to soils. Freshwater : 2.3 x 1026 cells ƒ Total biomass of prokaryotes in aquatic habitats and oceanic sub-surfaces : ~ 60-100% of the total C found in plants ƒ The higher cellular production of prokaryotes is found in aquatic ecosystems : >1030 cells/year ƒ Photosynthetic and heterotrophic microorganisms play a key role in ecosystem functioning and the global biogeochemical cycles. Phytopk fix up to 50 GtC/year vs. BP averages 50% of the PP

Aquatic Microorganisms Abundance ™ In 1 ml of water samples (oceans, lakes, estuaries, etc) : Heterotrophic prokaryotes Photosynthetic prokaryotes Protozoan (Flagellates, Ciliates) Microalgae Zooplankton Fishes

™ Quid of Viruses ?

1 000 000 cells 100 000 cells < 10 000 cells < 5 000 cells 1030 viruses in aquatic habitats The viral string of pearls is ~10 million light years long

Phages are probably the most abundant life forms on Earth

Aquatic Viruses Abundance Viruses represent 5% of the prokaryotic biomass Viruses contain more carbon than 75 million blue whales (~280 Mt)

From Suttle 2007

Aquatic Viruses The main domains of phage research

™ The environment (ecology and pollution) ™ The bacterial pathogenicity ™ The food industry ™ The evolution ™ The genomic aspect ™ The phagotheraphy

Aquatic Viruses Virus life cycle

Diet

Lysogenic cycle

Insertion Induction UV, nutriments, mutagens, environmental stress

Nutriments, Temperature, host physiology

Lytic cycle Diversity, population control, nutrient fluxes

Character acquisition

Aquatic Viruses Virus life cycle The most important life cycle is still not known in aquatic habitats Contradictory results dealing with lytic vs. lysogenic processes: - important spatial and time variability - important shifts from one to another (environmental factors) Viral-induced cell lysis has been the most studied to date 25-80% of viruses in a community are likely to be infectious There are ~1023 viral infections per second in the ocean 20 to 60% of member species are lysogens (i.e. contain prophages) The frequency of lysogeny varies among taxonomic groups

Aquatic Viruses Assessing the role of livings in the functioning of aquatic ecosystems require to be able to give answers to 3 basic questions :

¾ Which organisms are there and in which proportion ? ¾ What are organism metabolic and reproduction rates ? ¾ What kind of players are they in the functioning of ecosystems ?

Aquatic Viruses

Profondeur (m)

Abundance, distribution, dynamics

Geneva Lake 2004

2005

2006

Lake Bourget

High viral numbers are found in surface waters, in near-shore waters, in eutrophic waters, during productive seasons

Aquatic Viruses 10

Cell ml-1 1e+6 2e+6 3e+6 4e+6 5e+6 6e+6 7e+6

Depth (m)

20 30 40

Heterotrophic Bacteria 50

10

Part ml-1

Depth (m)

20

2.0e+7 4.0e+7 6.0e+7 8.0e+7 1.0e+8 1.2e+8

r= 0.48

30

p= 0.03 40

Viruses

n= 21

50 Mar

From Personnic 2007

May

Jul

Sep

Nov

Aquatic Viruses Microbial loop Fishes

Classical chain

virus

Protozoans

Zooplankton

Phytoplankton Bacteria Inorganic Nutrients

Organic Nutrients

Ecological Role of Aquatic Viruses Virus-induced mortality

50x1060

-1

-1

E. huxleyi (cell.ml )

100x103

Virus de E. huxleyi (part.ml )

120x103

From Jacquet et al. 2002

A

80x103 60x103 40x103 20x103

B

40x106 30x106 20x106 10x106 0 1

3

5

7

9

Temps (jours)

11

13

Ecological Role of Aquatic Viruses Virus-induced mortality

From Simek et al. 2001

From Weinbauer & Hofle 1998

Ecological Role of Aquatic Viruses Virus-induced mortality Viruses remove app.10 to 50% of prokaryotic biomass per day

Mortality by viruses equals grazing by small eukaryotic predators

Ecological Role of Aquatic Viruses Viruses and organic carbon release

From Wommack & Colwell 2000

Ecological Role of Aquatic Viruses Viruses and organic carbon release Cell leakage