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Research persons: Alexandra Dubini

Location: Carnegie, United States

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The single-celled green alga Chlamydomonas reinhardtii generates hydrogen by
fermentation under low oxygen conditions. Cells in photo are stained with
fluorescent dyes. Purple indicates DNA, green indicates flagella.

Photosynthesis produces the food that we eat and the oxygen that we breathe ―
could it also help satisfy our future energy needs by producing clean-burning
hydrogen? Researchers studying a hydrogen-producing, single-celled green alga,
Chlamydomonas reinhardtii, have unmasked a previously unknown fermentation
pathway that may open up possibilities for increasing hydrogen production.

C. reinhartii, a common inhabitant of soils, naturally produces small quantities
of hydrogen when deprived of oxygen. Like yeast and other microbes, under
anaerobic conditions this alga generates its energy from fermentation. During
fermentation, hydrogen is released though the action of an enzyme called
hydrogenase, powered by electrons generated by either the breakdown of organic
compounds or the splitting of water by photosynthesis. Normally, only a small
fraction of the electrons go into generating hydrogen. However, a major research
goal has been to develop ways to increase this fraction, which would raise the
potential yield of hydrogen.

In the new study by Dubini et al, published in the Journal of Biological
Chemistry, researchers at the Carnegie Institution’s Department of Plant
Biology, the National Renewable Energy Laboratory (NREL), and the Colorado
School of Mines (CSM), examined metabolic processes in a mutant strain that was
unable to assemble an active hydrogenase enzyme. The researchers, who include
Alexandra Dubini (NREL), Florence Mus (Carnegie), Michael Seibert (NREL),
Matthew Posewitz (CSM), and Arthur Grossman (Carnegie), expected the cell’s
metabolism to compensate by increasing metabolite flow along other known
fermentation pathways, such as those producing formate and ethanol as end
products. Instead, the algae activated a pathway leading to the production of
succinate, which was previously not associated with fermentation metabolism in
C. reinhardtii. Notably, succinate, a widely used industrial chemical normally
synthesized from petroleum, is included in the Department of Energy’s list of
the top 12 value added chemicals from biomass.

“We actually didn’t know that this particular pathway for fermentation
metabolism existed in the alga until we generated the mutant,” says Carnegie’s
Arthur Grossman. “This finding suggests that there is significant flexibility in
the ways that soil-dwelling green algae can metabolize carbon under anaerobic
conditions. By blocking and modifying some of these metabolic pathways, we may
be able to augment the donation of electrons to hydrogenase under anaerobic
conditions and produce elevated levels of hydrogen.”

Grossman points out that it makes evolutionary sense that a soil organism such
as Chlamydomonas would have a variety of metabolic pathways at its disposal.
Oxygen levels, nutrient availability, and levels of metals and toxins can be
extremely variable in soils, over both the short and long term. “In such an
environment”, Grossman says, “these organisms must evolve flexible metabolic
circuits; the variety of conditions to which the organisms are exposed might
favor one pathway for energy metabolism over another, which would help the
organism compete in the soil environment over evolutionary time.”

Grossman led the effort to generate a fully sequenced Chlamydomonas genome,
which has allowed researchers to identify key genes encoding proteins involved
in both fermentation and hydrogen production. Grossman feels that it is of
immediate importance to generate new mutant strains to help us understand how we
may be able to alter fermentation metabolism and the production of hydrogen.
NREL’s Michael Seibert, the project’s Principal Investigator, observed that “the
overarching goal of the work is to gain a fundamental understanding of the total
suite of metabolic processes occurring in Chlamydomonas and how they interact;
this discovery effort will lead to the development of novel ways to produce
renewable hydrogen and other biofuels, which will benefit all of us”.

“These are really exciting times in the field,” says Matthew Posewitz. “The
tools developed at Carnegie and by other groups in the field are presenting
unprecedented opportunities for scientists to make important advances in our
understanding of the basic biology of organisms such as Chlamydomonas.”

As an energy source to potentially replace fossil fuels, hydrogen would greatly
reduce the emission of greenhouse gases. Proponents of algal-based hydrogen
production point out that, unlike ethanol produced from crops, it would not
compete with food production for agricultural land.