SYMBIOSIS - Cyanobacteria - page 373

differentiation in free-living cyanobacteria on nitrogen starvation) has been proposed by Meeks et al.
(1988). The evidences in favour of this hypothesis are that (i) vegetative cells of symbiotic cyanobacteria
(growing in association with A . punctatus , Azolla caroliniana , Zamia skinneri and Gunnera manicata )
possess cyanophycin and phycobiliproteins signifying that the presence of these nitrogen reserves
does not in any way cause a nitrogen defi ciency; (ii) the heterocysts of cyanobacteria in association
with A . punctatus and Azolla sp. contain phycobiliproteins, a feature that is entirely lacking in the
heterocysts of free-living cyanobacteria, (iii) the end product of nitrogen fi xation translocated in the
symbiotic forms is ammonia whereas in free-living cyanobacteria glutamine is translocated to adjacent
vegetative cells and (iv) the symbiotically associated Nostoc continues to differentiate heterocysts at a
high frequency even though the vegetative cells are present in exogenous ammonia secreted by it. In
this respect the symbiont is suggested to possess a different regulatory mechanism from the free-living
cyanobacterial sensing and signalling pathway to nitrogen deprivation. Evidences in support of such
a mechanism are the isolation of mutants of N . punctiforme defective in nitrate assimilation. Nitrate
neither supported growth nor repressed heterocyst differentiation. Symbiotic tissues of A . punctatus
established with the above mutants responded differently in presence of nitrate by the repression of
nitrogenase (probably heterocyst differentiation as well). This has been explained on the basis that
the plant partner ceases to produce signals controlling cellular differentiation in the symbiont. On
this basis, Meeks (1998) suggested the existence of a combined nitrogen-independent sensing and
signalling pathway in the heterocyst differentiation of the symbiont. Further, it is suspected that the
symbiotic sensing and signalling pathway overtakes the combined nitrogen deprivation sensing
and signalling system (that operates in the free-living growth state) so that heterocysts continue to
differentiate even in presence of nitrogen derived ammonium. Strains (mutants or natural isolates)
of Nostoc that lack symbiotic sensing and signalling pathway, however, fail to form a successful
nitrogen-fi xing symbiotic association with A . punctatus because of their failure to respond to the
plant signals that initiate enhanced level of heterocyst differentiation.
The organization of nif genes in Nostoc sp. 7801 in symbiotic association with A . punctatus as
revealed by restriction fragments is consistent with a contiguous nifHDK operon where as nifD and
nifK genes are nominally separated by an unknown length of intervening sequence in cultured
isolates and Anabaena sp. strain PCC 7120 (Meeks et al ., 1988).
The importance of nitrogen fi xation by mosses has been emphasized. Nitrogen fi xation reported
from Swedish mires was shown to be due to endophytic Nostoc sp. present in the hyaline cells of
leaves of Sphagnum sp. (Granhall and Hofsten, 1976; Solheim and Zielke, 2002). This is the only report
on the probable existence of a cyanobiont in a moss species. No further details are available about
this association. In all the other reports on nitrogen fi xation by mosses, the symbionts are reported to
be epiphytic (Solheim and Zielke, 2002). Sphagnum riparium and Drepanocladus exannulatus exhibited
peaks in light-dependent nitrogen fi xation around 16ºC and 11ºC (Basilier et al ., 1978). Pleurozium
schreberi , a feather moss ubiquitous in boreal forests that accounts for 90% of the total cover, has been
shown to be associated with Nostoc sp. (DeLuca et al ., 2002). Zackrisson et al . (2004) emphasized that
this association exerts a great impact on the nitrogen cycle of mature boreal forests. The epiphytic
association of a number of cyanobacteria with many moss genera has been examined by the use of a
variety of microscopic techniques (confocal laser scanning microscopy, epifl uorescence and scanning
microscopy). By confocal laser scanning microscopy of moss genera Sanionia uncinata , Calliargon
richardsonii and Bryum pseudotriquetrum (from Norway) and Hyloconium splendens (from Sweden),
it was possible to see deeper layers and create three-dimensional images. In S . uncinata the leaves
have formed grooves completely enclosing the cyanobacteria. The spaces between stem and leaves
of C . richardsonii serve as good sites for the colonization of the cyanobacteria. The prevalence of