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Sugar’s Role in Climate Change

Phytoplankton

Phytoplankton living in the surface waters of the oceans are responsible for absorbing up to 40% of all of the carbon that becomes incorporated into living things.

By Christel Hassler

Marine plankton account for up to 40% of carbon absorbed by all living things, but their growth is limited in half of the world’s oceans by iron bioavailability. New research has found that marine plankton can produce sugars that improve iron bioavailability – and hence plankton growth.

Phytoplankton living in the surface waters of the oceans are responsible for absorbing up to 40% of all of the carbon that becomes incorporated into living things, so their health, reproduction and productivity are of huge significance in regulating the amount of CO2 in the atmosphere.

Just like land plants and animals, the health of phytoplankton depends on access to trace elements and minerals such as zinc, cobalt and particularly iron. New research has found that the availability of iron to phytoplankton depends on complex sugars released by microorganisms, perhaps even by the phytoplankton themselves. The sugars interact with iron and provide it to the phytoplankton in a form they can use.

Iron is a critical micronutrient for phytoplankton. It plays a pivotal role in many of the enzymes and biochemical compounds that support critical biological functions such as photosynthesis and the uptake of other nutrients.

But large areas of our oceans, including the Southern Ocean, are defined as “high nutrient, low chlorophyll” (HNLC) regions where phytoplankton biomass is remarkably low despite containing high levels of nutrients. Most of these areas are extremely “anaemic” in iron, and this lack of iron restricts phytoplankton growth.

In other oceanic regions defined as “low nutrient, low chlorophyll” (LNLC) it is mostly the lack of nitrogen, in the form of nitrate, that limits the growth of phytoplankton. But iron is essential for the biological uptake of nitrogen. In LNLC regions, such as the North Atlantic and the Coral Sea, iron is also a limiting nutrient.

Over previous decades studies have shown that iron controls the abundance and diversity of phytoplankton in about half the ocean. It is an essential element for the global carbon cycle, the regulation of our climate and allocation of oceanic resources. If we can understand how iron controls phytoplankton it will help us to predict how phytoplankton will respond to climate change.

Not all iron can be used by phytoplankton to support their requirements – it has to be in the right form. Understanding what controls iron bioavailability in iron-limited regions of the world’s oceans is the challenge we are tackling.

Despite many studies, the factors controlling iron’s bioavailability to phytoplankton are not well-understood because the chemistry of iron in surface ocean water and its association with microorganisms is extremely complex and dynamic. The bioavailability of iron is influenced by its chemical forms and by the way it is used and released by phytoplankton and other microorganisms such as bacteria and viruses. The microbes affect bioavailability directly by releasing natural materials that can react with iron and change its chemistry.

Each member of the microbial community in the ocean has a different growth requirement for iron and a different strategy for coping with iron limitation. Where iron is limited, microorganisms battle each other for it. Only the most successful in securing their iron needs will thrive.

Studies have shown that more than 95% of the iron in the ocean is bound up with organic materials known as ligands. Unfortunately, the nature of marine iron-binding organic ligands is not well understood.

We know, for instance, that small ligands known as siderophores are released by some bacterioplankton when iron is limiting. It requires lots of energy to produce siderophores, but they help microorganisms take up iron so well that it is worthwhile.

However, siderophores are present in such low amounts that there are not enough of them in the ocean to account for all the iron-binding organic ligands present. Hence it is unlikely that siderophores alone control iron bioavailability to phytoplankton, which do not produce siderophores themselves.

A collaboration between researchers from Australia, The Netherlands and New Zealand has now revealed a new type of organic ligand that seems to be central to the bioavailability of iron to phytoplankton in the Southern Ocean.

Most marine bacterioplankton and phytoplankton produce polysaccharides (sugar polymers) that are either stored as energy reserves or released as exopoly­saccharides that coat the outside of the cell and assist in colony formation, attachment to surfaces, nutrient attraction and protection from extreme temperatures. Poly­saccharides are so widely produced by microorganisms that they represent 10–50% of dissolved marine organic carbon. Their distribution through the ocean layers reveals that poly­saccharides are reactive compounds. In fact, recent studies show that high concentrations of microbial polysaccharides can improve the growth of phytoplankton.

We used both laboratory phytoplankton cultures and natural plankton communities from the Southern Ocean to demonstrate that microbial polysaccharides improve iron bioavailability to phytoplankton. We estimated iron bioavailability by measuring the amounts of iron inside phytoplankton cells when different organic materials were present while the total amount of iron was kept at a constant level.

By separating the natural plankton community into different sizes using filters with pores of different sizes, we were able to tell the difference between iron bioavailability to large phytoplankton cells and smaller bacterioplankton cells.

There were some striking differences. While well-known siderophores decreased iron bioavailability to both groups, a simple sugar called glucuronic acid increased iron bioavailability to phytoplankton but decreased it to bacterioplankton.

Similar observations were made at two different sites with different plankton communities. This suggested that the increased bioavailability of iron to phytoplankton in the presence of glucuronic acid was a common feature in the Southern Ocean.

It also seems likely that microbial polysaccharides are important in keeping iron bioavailable for phytoplankton, giving them a growth advantage in iron-limited oceanic regions.

Given our promising results with natural microbial communities, we decided to investigate the effect of two sugars – glucuronic acid and the polysaccharide dextran – on iron bioavailability in a more controlled setting. In the laboratory we also studied a natural exopolysaccharide from the Southern Ocean to represent the natural organic material likely to be found there. We used pure laboratory cultures of two different Southern Ocean phytoplankton that are likely to have different iron requirements and strategies to take it up, and compared how fast iron was taken into cells.

Both the glucuronic acid and the dextran improved iron bioavailability to the two laboratory cultures tested. The natural exopolysaccharide was the only sugar to mildly reduce iron bioavailability. However, this reduction was much smaller than when the siderophore was present. This suggests that the observation that sugars maintain the pool of bioavailable iron to phytoplankton is not restricted to glucuronic acid.

Our results broaden the theory about how iron controls phytoplankton abundance, biodiversity and activity. We have shown that biologically produced polysaccharides help to control the forms of iron present, and hence its bioavailability. Our study demonstrated that polysaccharides play a critical role in maintaining the bioavailable iron pool for phytoplankton.

The importance of biologically produced polysaccharides is widespread since they are present in all aquatic systems. Polysaccharides can bind essential micro­nutrients other than iron, such as zinc and cobalt.

The possibility that large phytoplankton produce polysaccharides to control their environment in the same way that bacterio­plankton produce siderophores to control iron bioavailability requires additional research.

Christel Hassler is Chancellor's Post Doctoral Research Fellow with the University of Technology Sydney’s Plant Functional Biology and Climate Change Cluster. The research described here was a collaboration with the Royal Netherlands Institute for Sea Research, CSIRO, the Center for Australian Weather and Climate Research and New Zealand’s National Institute of Water and Atmospheric Research, and was published in the Proceedings of the National Academies of Science. Co-authors are V. Schoemann, E.C.V. Butler, C.A. Mancuso Nichols, M. Doblin, P.J. Ralph and P.W. Boyd.