Oceans of ArchaeaSeminar presentation by

Simon Krattinger

based on the paper byEdward F. DeLong

Oceans of ArchaeaAbundant oceanic Crenarchaeota appear to derive from thermophilic ancestors

that invaded low-temperature marine environments

ASM News 69, 2003, 503-511 (October issue)

Introduction

Earth‘s microbiota is remarkably pervasive:

high temperature low and high pH high salinity low water availability

Archaea: especially suited to exploit environmental extremes

But: Archaea exist also in a wide variety of terrestial, freshwater and marine habitats, sometimes in very high abundance.

Introduction

Archaea seem to have derived from thermophilic ancestors that invaded diverse low-temperature environments.

Overview of Archaea

First recognized in the late 1970s by Carl Woese and Ralf Wolfebased on ribosomal RNA analyses

Well-known and cultivated Archaea generally fall into serveral major phenotypic groups:

• Halophilic archaea (haloarchaea)• Strictly anaerobic methanogenic archaea (produce most of the methane present in the atmosphere)

• Heat- and acid- loving thermophiles and thermo- acidophiles (hydrothermal vents, deep subterranean environments)

Cultivated members of Crenarchaeota consist entirely of thermophilic species.

Although Archaea were thought to preferentially occupy environments thatare inhospitable to Eucarya and Bacteria, their ecological and physiologicaldiversity turns out to be far greater than previously assukmed.

1992: PCR-based, rRNA-gene surveys of mixed microbial populations fromopen ocean and costal marine waters.

Result: A lot of different Archaea were found, contributing significantly to thetotal extractable rRNA in marine surface waters.

Surprise: Members of almost any archaeal group could be found in cold, aerobic habitats of costal and open waters as well.

Four groups of planktonic marine Archaea

Four groups of planktonic marine Archaea

Group I: (Crenarchaeota)Group II: (Euryarchaeota)Group III: found in waters below the photic zone (related to Thermoplasmatales)Group IV: inhabit deep ocean waters (related to haloarchaea)

Antarctic Crenarchaeota in winter surface water sometimes comprise 20%of total microbial rRNA (cultivated Crenarchaeota have optimal growth temperature of 80°C).

Study of temperate waters in the North Pacific Ocean

Estimates from these cell counts indicate that planktonic Crenarchaeotamake about 20% of all the bacterial and archaeal cells found in the sea.

Abundance of planktonic Archaea at the Hawaii Ocean Time series station as a function of depth, determined by fluorescence insitu hybri-dization counts. Percentage of Marine Group I Archaea relative to total microbial counts in 2A is indicated by color; red, 40% of cell total; dark blue, 0% of cell total.

Figure 2B shows the distri-bution of cell types deter-mined by FISH, averaged over one year. Crenarchaeota refers specifi-cally to Marine Group I Archaea, and Euryarchaeota refers specifically to Marine Group II Archaea.

From Karner, M, E. F. DeLong, and D. M. Karl. 2001. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409: 507–

510, with permission.

Another Surprise – an Archaeal Symbiont of Sponges,Cenarchaeum symbiosum

This Archaea (Crenarchaeota) lives within the costal marine sponge Axinella mexicana at temperatures of about 10°C.

C.symbiosum is detectable only within the sponge and not in the surrounding seawater or associated with other sponges.

C.symbiosum can be successfully maintained in laboratory aquaria within the tissues of its host and is therefore a good model organism to study marine, cold-loving (psychrophilic) Archaea.

The marine sponge Axinella mexicana and its archaeal symbiont, Cenarchaeum symbiosum.

3A Axinella mexicana a bright red demosponge found off the California coast.

3B Axinella mexicana maintained in laboratory aquaria.

3C FISH experiment showing C.symbiosum population present in the sponge tissues (in green). Many of the C. symbio-sum cells are visibly dividing.

Physiological Ecology of Oceanic Archaea

Relatively little is known about the physiology of oceanic Archaea species (no pure cultures are available yet).

Archaeal lipids: GDGTs (Glycerol dibiphytanyl glycerol tetraethers) are commonly found archaeal lipid structures

Archaeal lipid structures found in marine plankton and sediments. GDGT, glycerol dibiphytanyl glycerol tetraether. The most common forms found in marine plankton, incorporating sidechains a, or d and e, are GDGTs I and VIII. Modified after S. Schouten, E.C.Hopmans,

R.D.Pancost, and J.S.S.Damste’. 2001.

Widespread occurrence of structu-rally diverse tetraether membrane lipids: Evidence for the ubiquitous presence of low-temperature rela-tives of hyper-thermophiles. Proc. Natl. Acad. Sci. USA 97:14421–14426, Copyright 2001, National Academy of Sciences, U.S.A.

Physiological Ecology of Oceanic Archea

Marine planktonic Archaea include a novel ether lipid, called crenarchaeol, which contains a six-membered cyclohexyl ring.

This change from the standard, five-membered ring (found in thermophilic archaeal lipids) adds a kink in the tetraether chains, rendering the membrane structures they form more fluid at lower temperatures.

Carbon source of marine Archaea

Planktonic Archaea use either algal carbohydrates, proteins or dissolved bicarbonate and thus do not indicate whether these Archaea are auto- or heterotrophs.

Deep-water Crenarchaeota are incorporating disolved CO2 as their main carbon source.CO2-fixation (13CO2 isotope tracer-labeling).

Archaea may therfore represent an unexpected source of primary productivity in the sea.

The energy source of these organisms is not yet known.

Genomics of Ocean Archaea

The genome of C.symbiosum is sequenced.

Although the DNA polymerase amino acid sequence most closely resemblesthermostable DNA polymerase from other hyperthermophilic Crenarchaeota,the enzyme itself is not thermostable. It is inactivated at abot 40°C.

What extraordinary event led to the wide distribution of Crenarchaeota in habitats ranging from boiling water in hot springs of 100°C to frigid polar waters of - 1.8°C ?

Evolutionary Origins of Oceanic Archaea

Marine Archaea once lived in anoxic, high-temperature habitats.

Different lineages within the Crenarcheota adapted to low-temperture environments.