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CARBON CYCLE

Quick burial at seaCaroline A. Masiello

The amount of river-borne carbon that is buried upon reaching the sea affects Earth’s atmospheric composition. A study of rivers draining the Himalaya shows that carbon burial may occur more efficiently than was thought.

It’s a popular misconception that the con-centration of oxygen in Earth’s atmosphere is controlled by photosynthesis. Photosynthesis is certainly the source of atmospheric O2, but the amount it produces is in almost perfect balance with the amount consumed through the respiration of living organisms. It is only when organic matter is buried in ocean sediments, and so ceases to be decomposed, that atmospheric O2 can accumulate. This burial process also reduces the levels of the greenhouse gas carbon dioxide released into the atmosphere. The exact rate of organic-matter burial is therefore a significant deter-minant of atmospheric composition, and thus global climate, over geological timescales.

On page 407 of this issue, Galy et al.1 bring a new perspective on how organic carbon is stored in sediments. They show that the Ganges–Brahmaputra river system, which drains the Himalaya, interacts with the sediments deposited by the rivers’ waters in the Bay of Bengal — the ‘Bengal fan’ — so as to store organic carbon more efficiently than studies on other river systems had suggested would be the case.

The fact that organic matter can be stored at all in ocean sediments is something of a surprise. Heterotrophic organisms (those that acquire their carbon from other organic mat-ter, rather than synthesizing it themselves from inorganic sources) operate highly efficiently in the oceans, tightly recycling carbon and nutri-ents in the ocean’s surface layers. Less than 1% of photosynthesized organic matter makes it down to the surface of ocean sediments2, and what carbon does hit the seafloor enters a voracious ecosystem that makes short work of almost all of it3. The little burial of organic matter that does take place occurs in river del-tas and at continental margins. In addition, rivers deliver more than enough carbon to the oceans to account for the total amount of car-bon stored in sediments4. These two facts have long raised suspicions that terrestrially derived organic matter is a significant source of the car-bon preserved in marine sediments.

But data from rivers and coastal sediments have created a more complex picture. In par-ticular, measurements made in the world’s largest river system, the Amazon, have shown that even the strongest bonds between miner-als and organic matter formed in soils can be broken during transport and deposition at the river–ocean margin. This causes terrestrial car-bon in mineral surfaces to be replaced, at least

in part, by marine carbon5. Indeed, the fan of sediment spreading out from the mouths of the Amazon has been called a “gigantic sedimen-tary incinerator”6 for its efficiency at destroy-ing both marine and terrestrial organic matter, preventing their burial at sea. There had been hints that other types of river — in particular, mountainous rivers on active tectonic margins such as those draining the Himalaya — export and store carbon differently from the Ama-zon7,8. But these rivers are individually small, making it difficult to place their stories in a globally significant context.

In their studies of the Ganges–Brahma-putra system, Galy et al.1 use the relationship between organic-carbon content and the ratio of aluminium to silicon in river and Bengal Fan sediments as a marker for the amount of organic matter these particles contain. They find that this relationship remains the same from the rivers’ youthful stages right through to sediment deposition in the ocean (Fig. 1). Coupling this information with earlier stud-ies using sedimentary biomarkers that showed no evidence of the storage of marine organic carbon in Bengal-fan sediments9, Galy et al.1 conclude, reasonably, that the terrestrial

organic matter is stored in the Bengal fan very efficiently — in contrast to the picture of destruction at the mouths of the Amazon.

The authors attribute this efficiency to the Bengal fan’s rapid sedimentation rate, which restricts the sediments’ exposure to oxygen, effectively cutting off microbial decomposi-tion of organic matter. They further argue that the driver for the rapid sedimentation is the fast erosion resulting from tectonic uplift in the Himalaya, an argument that meshes with hypotheses previously published for much smaller rivers draining tectonically active margins7.

But is this all there is to it? Those of us who study the river transport of organic matter to the ocean make the unstated assumption that carbon loading does not vary with the soil properties of the particular river basin. We assume that rocks break apart into soil miner-als, soil minerals load with organic matter, and organically coated minerals are exported to rivers by essentially the same mechanisms the world over, with soil type and degree of devel-opment influencing the final storage outcome only insignificantly. Yet soil scientists know that soil mineralogy has an important part in determining the mechanisms and durability of organo-mineral bonds: for example, the effec-tiveness of carbon storage in soil varies greatly with the degree of soil weathering10.

The Amazon and Ganges–Brahmaputra river systems are ideal for testing the effect of river-basin soils on the storage of organic carbon in delta sediments, because they drain environments that represent two extremes of soil development. The Amazon basin is domi-nated by Oxisols, the most highly weathered

Figure 1 | From mountains to the sea. In the Ganges–Brahmaputra river system, particles eroded from the Himalaya weather and become loaded with organic carbon in the ecosystems of the drainage basin. With their coatings of terrestrial carbon intact, these particles are delivered to the ocean floor off the coast of Bangladesh. Galy and colleagues’ study1 indicates that the carbon content of these sediments is efficiently preserved in the Bengal sedimentary fan, preventing this carbon from being released to the atmosphere as CO2.

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type of soil, whereas the Ganges–Brahmaputra basin is dominated by Inceptisols, one of the least weathered soil orders. Understanding the influence of river-basin soils on the storage of carbon in ocean sediments will require the effective integration of soil data into the field of oceanography. Carbon-coated minerals travel from mountains through ecosystems to rivers and ocean sediments: perhaps understanding these particles’ history will help us predict their sedimentary fate. ■

Caroline A. Masiello is in the Department of Earth Science, Rice University, Mail Stop 126, 6100 Main Street, Houston, Texas 77005, USA.e-mail: masiello@rice.edu

MICROBIOLOGY

Pathogen drop-kickSuzanne Pfeffer

To set the scene for its replication, the bacterium Legionella pneumophila exploits its host cells’ Rab1 protein. This pathogen seems to use minimal resources to mimic the normal cycle of Rab1 activity.

The bacterium Legionella pneumophila is the main agent responsible for both Legion-naires’ disease, which leads to pneumonia, and Pontiac fever, an illness that resembles acute influenza. This pathogen is engulfed by immune cells known as macrophages and, once inside, exploits proteins mediating intracellular trafficking to form an organelle called an L. pneumophila-containing vacuole, or LCV. The bacterium then replicates inside the LCV. Two papers1,2, including one by Ingmundson and colleagues that appears on page 365 of this issue, provide insight into how L. pneumophila uses one host-cell protein to form LCVs.

Among the proteins that mediate intra-cellular trafficking are Rabs; the human genome encodes about 70 of these pro-teins3. Rabs are involved in organizing membranes for the formation of vesicu-lar carriers, the transport of these vesi-cles between cellular compartments and vesicle fusion with the membrane of tar-get cellular compartments. Rab proteins interconvert between an active, GTP-bound state and an inactive, GDP-bound form. To activate a Rab protein, enzymes known as GEFs exchange its bound GDP nucleotide for a GTP, whereas for Rab inactivation, enzymes known as GAPs help Rabs hydrolyse Rab-bound GTP to produce GDP.

So the Rab cycle of activity goes as follows. An active, GTP-bound Rab uses two 20-carbon-long ‘anchors’ to bind to the membrane surface of dis-tinct organelles. There, it organizes the formation of functional membrane

microdomains. GAP-stimulated hydro lysis of Rab’s GTP to GDP follows, allowing a cyto-plasmic protein called GDI to bind to the inactive Rab and extract it from membranes4. Afterwards, another protein, GDI displace-ment factor, or GDF, releases Rab from GDI, and GEF enzymes then mediate the exchange of Rab’s GDP molecule for a GTP, preparing Rab for its next cycle of activity5,6.

Ingmundson et al.1 and the authors of a recent Science paper2 demonstrate that, to harness the host-cell cycle of Rab activity, an L. pneumophila protein known as DrrA functions as both a GDF and a GEF. This pathogen specifically targets Rab1, which normally mediates vesicle transport from the endoplasmic reticulum to the Golgi complex.

Previous work7,8 had shown that DrrA can both recruit Rab1 to LCVs and activate it. Furthermore, the carboxyl terminus of DrrA (that is, amino-acid residues 451–647) has been shown to function as a Rab1-specific GEF in vitro, explaining the ability of this protein to activate Rab1 (ref. 7). In living cells, however, this region of DrrA was insufficient to recruit Rab1 to LCVs.

These observations led the authors1,2 to test whether DrrA also functions as a GDF to release Rab1 from GDI and recruit it to LCVs. Ingmundson et al. find1 that amino-acid resi-dues 1–500 of DrrA — which lack GEF activity — can efficiently release Rab1 from GDI. This suggests that two separate regions within a sin-gle L. pneumophila protein contain GDF and GEF activities, allowing it to drop-kick Rab1 off GDI and onto adjacent membranes in an active form (Fig. 1).

Structurally, such an arrangement makes sense. The so-called ‘switch’ domains that participate in GTP/GDP nucleotide binding are the only parts of Rab proteins to change conformation between the GDP- and GTP-bound states. So proteins such as GDI that spe-cifically interact with the GDP-bearing form of the ‘switchable’ proteins must recognize the status of the switch domains; the crystal struc-ture9 of a Rab bound to GDI shows that this

is the case. Similarly, to catalyse nucleotide exchange, a GEF must also access the switch domains. Thus, with GDI tightly bound to Rab proteins, GDF must move the GDI off the switch domain to permit a GEF to do its job.

A GDF can localize a Rab protein to a specific membrane after dissociating it from a GDI (ref. 10). DrrA is found on the inner leaflet of the infected host-cell membrane and, in cells that express DrrA exogenously, this protein can mis-target Rab1 so that it also localizes to the cell membrane7,8. It will be interesting to determine how DrrA localizes to the inner cell membrane in the first place.

Ingmundson et al.1 also show that another L. pneumophila protein, LepB, is a Rab1-specific GAP enzyme. Thus, these bacteria seem to be self-sufficient in conducting the Rab1 cycle: they build a functional membrane microdomain by recruiting and locally acti-vating Rab1, and, when appropriate, disas-semble this microdomain using a bacterially encoded GAP (Fig. 1). The bacteria eventu-ally return Rab1 to host-cell service, which might in itself be beneficial to a productive infection process.

What are the main functions of Rab1

Figure 1 | How Legionella pneumophila exploits host-cell Rab1 protein. In the host-cell cytoplasm, the inactive, GDP-bearing Rab1 associates with GDI. This complex is recognized by the DrrA protein of L. pneumophila, which localizes to the inner leaflet of the cell membrane. Two studies1,2 find that one region of DrrA acts as a GDF, releasing Rab1 from GDI, whereas another domain of this protein functions as a Rab1-specific GEF to activate Rab1 by catalysing the exchange of its associated GDP for a GTP. The active Rab1 can then anchor into the adjacent membrane to organize the formation of a functional membrane microdomain. Later, another L. pneumophila protein, LepB, stimulates the hydrolysis of Rab1-bound GTP to GDP and inorganic phosphate (P), thereby inactivating Rab1.

1. Galy, V. et al. Nature 450, 407–410 (2007).2. Hedges, J. I. & Keil, R. G. Mar. Chem. 49, 81–115 (1995).3. Witte, U., Aberle, N., Sand, M. & Wenzhofer, F. Mar. Ecol.

Prog. Ser. 251, 27–36 (2003).4. Hedges, J. I., Keil, R. G. & Benner, R. Org. Geochem. 27,

195–212 (1997).5. Keil, R. G., Mayer, L. M., Quay, P. D., Richey, J. E. & Hedges,

J. I. Geochim. Cosmochim. Acta 61, 1507–1511 (1997).6. Aller, R. C. & Blair, N. E. Cont. Shelf Res. 26, 2241–2259

(2006).7. Milliman, J. D. & Syvitski, J. P. M. J. Geol. 100, 525–544

(1992).8. Blair, N. E., Leithold, E. L. & Aller, R. C. Mar. Chem. 92,

141–156 (2004).9. Freeman, K. H. & Colarusso, L. A. Geochim. Cosmochim.

Acta 65, 1439–1454 (2001).10. Torn, M. S., Trumbore, S. E., Chadwick, O. A., Vitousek,

P. M. & Hendricks, D. M. Nature 389, 170–173 (1997).

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