Page 184 - Algae Anatomy, Biochemistry, and Biotechnology

Biogeochemical Role of Algae 167

spatial and temporal segregation of nitrogen fixation from photosynthesis, and a sequential pro-
gression of photosynthesis, respiration, and nitrogen fixation over a diel cycle are the strategies
used by these cyanobacteria. These pathways are entrained in a circadian pattern that is ultimately
controlled by the requirement for an anaerobic environment around nitrogenase. Light initiates
photosynthesis, providing energy and reductants for carbohydrate synthesis and storage, stimulat-
ing electron cycling through PSI, and poising the plastoquinone (PQ) pool at reduced levels. High
respiration rates early in the photoperiod supply carbon skeletons for amino acid synthesis (the
primary sink for fixed nitrogen) but simultaneously reduce the PQ pool further. Linear electron
flow to PSI is never abolished. The reduced PQ pool leads to a downregulation of PSII, which
opens a window for N 2 fixation during the photoperiod, when oxygen consumption exceeds
oxygen production. As the carbohydrate pool is consumed, respiratory electron flow through the
PQ pool diminishes, intracellular oxygen concentrations rise, the PQ pool becomes increasingly
oxidized, and net oxygenic production exceeds consumption. Nitrogenase activity is lost until
the following day.
A full temporal separation between oxygenic photosynthesis and nitrogen fixation occurs in
P. boryanum and O. limosa. Transcription of nitrogenase and photosynthetic genes are temporally
separated within the photoperiod, that is, nitrogenase is expressed primarily during the night. Nitro-
genase is contained in all cells in equal amounts. The onset of nitrogen fixation is preceded by a
depression in photosynthesis that establishes a sufficiently low level of dissolved oxygen in the
environment. Plectonema sp. has a versatile physiology that allows it to reversibly modulate uncou-
pling of the activity of the two photosystems in response to intracellular nitrogen status. Oscilla-
toria sp. initiates nitrogen fixation in the dark and performs it primarily in the absence of light.
In non-heterocystous cyanobacteria such as the filamentous Symploca sp. and Lyngbya maius-
cola, and the unicellular Gloeothece sp. and Cyanothece sp., the temporal separation does not need
a microaerobic environment. Phormidium sp. and Pseudoanabaena sp. are other examples of
cyanobacteria fixing only under microanaerobic conditions. Under contemporary oxygen levels,
all of these organisms are relegated to narrow environmental niches.
In heterocystous cyanobacteria, such as Anabaena sp. and Nostoc sp., a highly refined special-
ization spatially separates oxygenic photosynthesis from N 2 fixation. Here, nitrogenase is confined
to a microanaerobic cell, the heterocyst, characterized by a thick membrane that slows the diffusion
of O 2 , high PSI activity, loss of division capacity, absence of PSII (that splits the water forming O 2 ).
This cell differentiates completely and irreversibly 12–20 h after combined nitrogen sources are
removed from the medium. The development of these cells, formed at intervals between vegetative
cells, is a primitive form of cell differentiation. In this process, all PSII activities are gradually lost,
and the proteins involved in oxygenic photosynthesis are degraded, whereas PSI activity is main-
tained. Simultaneously, the production of active nitrogenase is triggered. Nitrogen fixation is
localized specifically in heterocysts, and light is used for cyclic electron flow around PSI to
maintain a supply of ATP for the process. The primary organic nitrogen product (glutamate) is
exported to adjacent vegetative and photooxygenic cells, while carbon skeletons, formed by the
respiratory and photosynthetic processes in the latter cells, are translocated to the heterocysts. In
some heterocystous cyanobacteria such as Anabaena variabilis, under anaerobic conditions, a
different Mo-dependent nitrogenase can be synthesized inside vegetative cells. This nitrogenase
expresses shortly after nitrogen depletion, but prior to heterocysts formation, and can support the
fixed N needs of the filaments independent of the nitrogenase in the heterocysts.
8
The biotic nitrogen fixation is estimated to produce about 1.7 10 tons of ammonia per year,
7
whereas atmospheric and industrial nitrogen fixation produce about 1.7 10 tons of ammonia
per year.
For all eukaryotic algae, the only forms of inorganic nitrogen that are directly assimilable are
2
þ
2
nitrate (NO 3 ), nitrite (NO 2 ), and ammonium (NH 4 ). The more highly oxidized form, nitrate, is the
most thermodynamically stable form in oxidized aquatic environments, and hence is the predomi-
nant form of fixed nitrogen in aquatic ecosystems, though not necessarily the most readily available