Gene Expression during Heterocyst Differentiation - Advances in Botanical Research - page 289

that in many cyanobacteria is provided by reduced ferredoxin (reviewed
in Luque & Forchhammer, 2008 ). The heterocyst contains high levels of
glutamine synthetase ( Dharmawardene, Haystead, & Stewart, 1973 ; Thomas,
Meeks, Wolk, Shaffer, & Austin, 1977 ), which respond to a specific pattern
of expression of the glnA gene encoding this enzyme ( Tumer, Robinson,
& Haselkorn, 1983 ; Valladares, Muro-Pastor, Herrero, & Flores, 2004 ), but
lacks glutamate synthase ( Martín-Figueroa, Navarro, & Florencio, 2000 ;
Thomas et al., 1977 ). Additionally, heterocysts isolated from Anabaena cylin-
drica can produce glutamine from glutamate and ammonia ( Thomas et al.,
1977 ). These observations suggested that an exchange of glutamine for
glutamate takes place between heterocysts and vegetative cells, in which
heterocysts provide the vegetative cells with fixed nitrogen in the form of
glutamine and the vegetative cells provide the heterocysts with the gluta-
mate needed for the glutamine synthetase reaction ( Thomas et al., 1977 ;
Wolk et al., 1976 ).
Not all the nitrogen fixed by the heterocyst is immediately exported.
The heterocysts conspicuously bear refractile polar granules in the neck
regions that form in the cell poles proximal to adjacent vegetative cells
( Fig. 8.1 A). These polar granules are made of cyanophycin ( Lang, Simon,
& Wolk, 1972 ), which is multi-L-arginyl-poly-(L-aspartic acid), a nitrogen
reserve that accumulates after nitrogenase activity peaks late in differen-
tiation ( Sherman, Tucker, & Sherman, 2000 ). However, the accumulation
of cyanophycin is not required for diazotrophic growth as demonstrated
by inactivation of cyanophycin synthetase(s) in both Anabaena variabilis
( Ziegler, Stephan, Pistorius, Ruppel, & Lockau, 2001 ) and Anabaena sp.
strain PCC 7120 ( Picossi,Valladares, Flores, & Herrero, 2004 ). On the other
hand, excessive accumulation of cyanophycin resulting from inactivation
of cyanophycinase, the first enzyme acting in cyanophycin degradation,
impairs diazotrophic growth ( Picossi et al., 2004 ).
2.4. Intercellular Molecular Exchange
As described above, the heterocyst provides the vegetative cells in the
filament with fixed nitrogen, and glutamine is a likely nitrogen vehicle
( Thomas et al., 1977 ; Wolk et al., 1976 ). Additionally, because the heterocyst
cannot perform the photosynthetic fixation of CO 2 , it needs to be fed with
reduced carbon, and sucrose is likely received from the photosynthetic veg-
etative cells as a source of reductant and energy ( López-Igual et al., 2010 ;
Vargas et al., 2011 ). Additionally, glutamate ( Thomas et al., 1977 ) and alanine
( Pernil et al., 2010 ) are likely transferred from vegetative cells to heterocysts.