Plant and Soil 137: 157-160, 1991.
© 1991 Kluwer Academic Publishers. Printed in the Netherlands. PLSO NL24
Are bacteria the third partner of the Azolla-Anabaena symbiosis?
FRANCISCO CARRAPI~O
Departamento de Biologia Vegetal, Faculdade de Ci6ncias de Lisboa, Campo Grande, Bloco C2, P-1700
Lisboa, Portugal
Key words: Azolla, bacteria, megasporocarps, symbiosis
Abstract
The development of the prokaryotic colony in Azolla filiculoides indicates that Anabaena azollae is
maintained through the life cycle of the fern and present in the leaves and megasporocarps. The same
biological pattern is applied to the bacteria that are also present in these structures and seems to follow
a development pattern identical to the cyanobacteria and probably can be considered the third partner
of this symbiotic association.
Introduction
The presence of bacteria in the Azolla leaves
were previously described by Grilli (1964) and
later referred by several authors, with some re-
serve, as an organism present in the leaf cavity of
the fern (Forni and Grilli Caiola, 1986; Gates et
al., 1980; Peters et al., 1978). In spite of this,
organism having been identified by the first time
by Bottomley in 1920 as Pseudomonas, the cor-
rect identification was done by Wallace and
Gates (1986) and included in the genus Arth-
robacter. Based on this identification Petro and
Gates (1987) suggest that these bacteria may be
the third component of the symbiosis. Using
different methods Carrapigo and Tavares (1987,
1989) have shown, by electron microscopy
studies, that these bacteria were always present
as a permanent member of the prokaryotic col-
ony at different stages of leaf development of
Azolla filiculoides and based on these data they
have also suggested that these bacteria were the
third partner of the symbiosis. At the same time
Forni et al. (1987, 1989) have identified by bio-
chemical tests several species of Arthrobacter
present in different species of Azolla, suggesting
the same hypothesis. The first references of the
presence of bacteria in sporocarps was made by
Peters and Calvert (1982) and by Tavares and
Carrapigo (1988). In this work, further research
was made on this symbiotic association, trying to
integrate and develop the understanding of the
relationship between the bacteria and the life
cycle of the fern.
Materials and methods
The Azolla filiculoides plants were collected in
Alcochete (70 km from Lisbon) and maintained
in cultivation chambers. The megasporocarps
were collected in April of 1987 and 1988 directly
from the wild and prepared for further studies.
Light and electron microscopy research were
made on dorsal lobe leaves and in mega-
sporocarps. For electron microscopy studies,
leaves were submitted to a double step fixation
process by 4% glutaraldehyde in 0.05 M cacody-
late buffer (pH 7.2) and in 1% OsO 4 in 0.05 M
cacodylate buffer (pH 7.4) with or without
ruthenium red (Carrapi~o and Tavares, 1989).
The leaves were dehydrated in acetone series
and embedded in Epon-Araldite (Mollenhauer,
1964). The megasporocarps were fixed in a fixa-
tive consisting of formaldehyde-glutaraldehyde
(2%-2.5%) in 50 mM PIPES buffer (pH 7.4) for