98
Filamentous cyanobacteria (Fay 1992) form N 2 -fixing heterocysts that are
differentiated from “vegetative” cells through a complex molecular and morphological sequence. They cannot revert to vegetative cells. Heterocyst-forming species
are comprised of chains of vegetative cells that perform oxygenic photosynthesis.
When fixed N 2 is in short supply, a chain of cellular events begins with expression
of a set of genes that leads to one of the cells differentiating irreversibly into a specialized cell with reduced O 2 concentrations and no photosystem II activity (Fay
1992). Heterocyst- forming genera found in marine environments include Anabaena,
Nodularia and Aphanizomenon and related species in estuarine waters (BentzonTilia et al. 2015; Paerl 2012; Stal 2009), a variety of species in mats including
Calothrix sp., Dichothrix sp. epiphytic on the pelagic macroalga Sargassum
(Carpenter 1972) and the diatom symbionts Richelia/Calothrix in oligotrophic
oceans (Villareal 1990, 1991).
Some nonheterocyst-forming cyanobacteria avoid O 2 inhibition by fixing at
night, as do most unicellular cyanobacteria. Genera such as Lyngbya, typically
found in mats, use this strategy (Bebout et al. 1987, 1994; Omoregie et al. 2004).
Trichodesmium is one of the major nonheterocyst-forming cyanobacteria in the
oceans. One of the most interesting and puzzling characteristics of Trichodesmium
is that it fixes N 2 only (or primarily) during the day, even though it is filamentous but
does not form heterocysts. This paradox of O 2 evolution and N 2 fixation has been the
subject of speculation and research for decades, and was first hypothesized to be
occur by differences in photosynthesis and O 2 evolution in the interior of aggregates
or bundles (Carpenter and Price 1976; Paerl and Bebout 1988). Although the mechanisms for this phenomenon remain unclear and are still controversial, several interesting aspects have been uncovered that may provide clues. Although at first glance,
Trichodesmium appears to be comprised of a filament of similar cells, the cells
along the trichome do have different characteristics in photosynthetic pigment fluorescence (“bright cells”) and protein (nitrogenase and cytochrome oxidase) content
as measured by immunological methods (Bergman and Carpenter 1991; Lin et al.
1998). These results were interpreted as reflecting partially differentiated cells,
termed “diazocytes” (Bergman and Carpenter 1991; Fredriksson and Bergman
1995) and it has been proposed that both temporal and spatial separation of photosynthesis and N 2 fixation are involved (Berman-Frank et al. 2001b). However, the
mechanisms involved are still not completely resolved (Stal and Zehr 2008; Zehr
and Capone 2020).
Chemotrophic N 2 -fixing microorganisms are found in the majority of marine
habitats examined to date (see Chaps. 4, 7 and 8). Many or most have been detected
by the presence of nif genes or transcripts and are not represented yet by closely
related cultivated isolates. Many marine heterotrophic N 2 -fixing bacteria reside in
anoxic or low- O 2 environments, such as sediments. The presence in oxic waters
presents somewhat of an enigma, because if they are actively fixing N 2 as several
studies suggest (see Chap. 4), it is unclear how they avoid O 2 inactivation.
Heterotrophic and chemautototrophic N 2 -fixing bacteria are often associated with
invertebrates such as shipworms (Lechene et al. 2007) and deep water corals
(Middelburg et al. 2015). Lucinid clams (Petersen et al. 2017) and even small
6 Factors Controlling N 2 Fixation
Filamentous cyanobacteria (Fay 1992) form N 2 -fixing heterocysts that are
differentiated from “vegetative” cells through a complex molecular and morphological sequence. They cannot revert to vegetative cells. Heterocyst-forming species
are comprised of chains of vegetative cells that perform oxygenic photosynthesis.
When fixed N 2 is in short supply, a chain of cellular events begins with expression
of a set of genes that leads to one of the cells differentiating irreversibly into a specialized cell with reduced O 2 concentrations and no photosystem II activity (Fay
1992). Heterocyst- forming genera found in marine environments include Anabaena,
Nodularia and Aphanizomenon and related species in estuarine waters (BentzonTilia et al. 2015; Paerl 2012; Stal 2009), a variety of species in mats including
Calothrix sp., Dichothrix sp. epiphytic on the pelagic macroalga Sargassum
(Carpenter 1972) and the diatom symbionts Richelia/Calothrix in oligotrophic
oceans (Villareal 1990, 1991).
Some nonheterocyst-forming cyanobacteria avoid O 2 inhibition by fixing at
night, as do most unicellular cyanobacteria. Genera such as Lyngbya, typically
found in mats, use this strategy (Bebout et al. 1987, 1994; Omoregie et al. 2004).
Trichodesmium is one of the major nonheterocyst-forming cyanobacteria in the
oceans. One of the most interesting and puzzling characteristics of Trichodesmium
is that it fixes N 2 only (or primarily) during the day, even though it is filamentous but
does not form heterocysts. This paradox of O 2 evolution and N 2 fixation has been the
subject of speculation and research for decades, and was first hypothesized to be
occur by differences in photosynthesis and O 2 evolution in the interior of aggregates
or bundles (Carpenter and Price 1976; Paerl and Bebout 1988). Although the mechanisms for this phenomenon remain unclear and are still controversial, several interesting aspects have been uncovered that may provide clues. Although at first glance,
Trichodesmium appears to be comprised of a filament of similar cells, the cells
along the trichome do have different characteristics in photosynthetic pigment fluorescence (“bright cells”) and protein (nitrogenase and cytochrome oxidase) content
as measured by immunological methods (Bergman and Carpenter 1991; Lin et al.
1998). These results were interpreted as reflecting partially differentiated cells,
termed “diazocytes” (Bergman and Carpenter 1991; Fredriksson and Bergman
1995) and it has been proposed that both temporal and spatial separation of photosynthesis and N 2 fixation are involved (Berman-Frank et al. 2001b). However, the
mechanisms involved are still not completely resolved (Stal and Zehr 2008; Zehr
and Capone 2020).
Chemotrophic N 2 -fixing microorganisms are found in the majority of marine
habitats examined to date (see Chaps. 4, 7 and 8). Many or most have been detected
by the presence of nif genes or transcripts and are not represented yet by closely
related cultivated isolates. Many marine heterotrophic N 2 -fixing bacteria reside in
anoxic or low- O 2 environments, such as sediments. The presence in oxic waters
presents somewhat of an enigma, because if they are actively fixing N 2 as several
studies suggest (see Chap. 4), it is unclear how they avoid O 2 inactivation.
Heterotrophic and chemautototrophic N 2 -fixing bacteria are often associated with
invertebrates such as shipworms (Lechene et al. 2007) and deep water corals
(Middelburg et al. 2015). Lucinid clams (Petersen et al. 2017) and even small
6 Factors Controlling N 2 Fixation