present in the leaf cavity and driven by the fern to modify some of its own
physiological and metabolic activities, which in turn change the fern’s own metabolic activity (Carrapiço 2010b, 2015a). One good example can be found in the
nitrogen metabolism associated to this symbiotic system shared by the host and
partners. The filaments of Anabaena present special cells (heterocysts) where nitrogenase converts atmospheric N2 into ammonia which is released into the leaf cavity
(Carrapiço 2010b, 2015a). It has been shown that intracellular ammonia pools of
symbiotically associated Azolla are five times greater than those of Azolla free of
cyanobacteria (Braun-Howland and Nierzwicki-Bauer 1990; Carrapiço 2010b,
2015a). The level of activity of ammonia-assimilating enzymes in the isolated
trichomes of the dorsal leaf cavity are much higher than those in Azolla leaves,
while some other activities in the Anabaena filaments are repressed to very low
levels. These results indicate that Azolla trichomes cells play an important role in the
nitrogen assimilation, which the cyanobiont fixes and releases into the cavity,
transferring it to the fern (Carrapiço 2010b, 2015a; Uheda, 1986).
This symbiosis is sustained throughout the fern’s life cycle, where the prokaryote
community (cyanobiont and bacteria) is always present and transferred from one
generation to the next, either in the dorsal leaf cavities or in the megasporocarps,
indicating the obligatory nature of the symbiotic association (Carrapiço 2010b,
2015a). It also suggests a phylogenetic coevolution of the symbionts and the host,
representing a good example of hereditary symbiosis and indicating that the complexity of the relationship between the host and the symbionts can be recognized as a
new level of biological organization in evolution, which can be included in the
concept of symbiogenic superorganism in biological and ecological terms
(Carrapiço 2010b, 2015a, b). This implies and involves the development and
acquisition of new metabolic and organic capabilities and also genetic sharing by
the partners in synchrony with the host, extending beyond the capability of each
individual forming the association or consortium (Carrapiço 2010b, 2015a, 2017,
2018).
With this concept, we have reinforced the idea that this symbiotic system works
in a synchronized way and can be considered a polygenomic entity (Fig. 27.4),
within which the different genomes operate together in a complementary and
synergistic way that benefits the whole (Azolla, cyanobateria and bacteria). It is as
if collectively they were a single living unity (a big one) acting as a symbiogenic
superorganism (Carrapiço 2012, 2015a, b). We might describe them as being either a
symbiome or holobiont (Carrapiço 2006, 2010b, 2015a, b, 2018; Guerrero et al.
2013; Sapp 2003; Suárez and Triviño 2019). This concept reinforces the principle
that eukaryote organisms are not genetically unique entities, and individual must
instead be seen as a complex biological ecosystem, formed by multiple
interdependent parts coexisting symbiotically within the whole (Carrapiço 2010b,
2015a). As previous referred, natural selection acts at the symbiome level, which is
composed of an integrated multigenomic genetic pool where all the genomes work
together for the whole (Carrapiço 2015a). Thus, we believe that the new metabolic
and organic capabilities acquired and developed by the partners establish a new level
of organization that goes beyond the individual capabilities of any individual
602
F. Carrapiço
physiological and metabolic activities, which in turn change the fern’s own metabolic activity (Carrapiço 2010b, 2015a). One good example can be found in the
nitrogen metabolism associated to this symbiotic system shared by the host and
partners. The filaments of Anabaena present special cells (heterocysts) where nitrogenase converts atmospheric N2 into ammonia which is released into the leaf cavity
(Carrapiço 2010b, 2015a). It has been shown that intracellular ammonia pools of
symbiotically associated Azolla are five times greater than those of Azolla free of
cyanobacteria (Braun-Howland and Nierzwicki-Bauer 1990; Carrapiço 2010b,
2015a). The level of activity of ammonia-assimilating enzymes in the isolated
trichomes of the dorsal leaf cavity are much higher than those in Azolla leaves,
while some other activities in the Anabaena filaments are repressed to very low
levels. These results indicate that Azolla trichomes cells play an important role in the
nitrogen assimilation, which the cyanobiont fixes and releases into the cavity,
transferring it to the fern (Carrapiço 2010b, 2015a; Uheda, 1986).
This symbiosis is sustained throughout the fern’s life cycle, where the prokaryote
community (cyanobiont and bacteria) is always present and transferred from one
generation to the next, either in the dorsal leaf cavities or in the megasporocarps,
indicating the obligatory nature of the symbiotic association (Carrapiço 2010b,
2015a). It also suggests a phylogenetic coevolution of the symbionts and the host,
representing a good example of hereditary symbiosis and indicating that the complexity of the relationship between the host and the symbionts can be recognized as a
new level of biological organization in evolution, which can be included in the
concept of symbiogenic superorganism in biological and ecological terms
(Carrapiço 2010b, 2015a, b). This implies and involves the development and
acquisition of new metabolic and organic capabilities and also genetic sharing by
the partners in synchrony with the host, extending beyond the capability of each
individual forming the association or consortium (Carrapiço 2010b, 2015a, 2017,
2018).
With this concept, we have reinforced the idea that this symbiotic system works
in a synchronized way and can be considered a polygenomic entity (Fig. 27.4),
within which the different genomes operate together in a complementary and
synergistic way that benefits the whole (Azolla, cyanobateria and bacteria). It is as
if collectively they were a single living unity (a big one) acting as a symbiogenic
superorganism (Carrapiço 2012, 2015a, b). We might describe them as being either a
symbiome or holobiont (Carrapiço 2006, 2010b, 2015a, b, 2018; Guerrero et al.
2013; Sapp 2003; Suárez and Triviño 2019). This concept reinforces the principle
that eukaryote organisms are not genetically unique entities, and individual must
instead be seen as a complex biological ecosystem, formed by multiple
interdependent parts coexisting symbiotically within the whole (Carrapiço 2010b,
2015a). As previous referred, natural selection acts at the symbiome level, which is
composed of an integrated multigenomic genetic pool where all the genomes work
together for the whole (Carrapiço 2015a). Thus, we believe that the new metabolic
and organic capabilities acquired and developed by the partners establish a new level
of organization that goes beyond the individual capabilities of any individual
602
F. Carrapiço