Trends in Microbiology
ReviewNitrogen fixation by marine cyanobacteria
Section snippets
N2 fixation in the oceans
The availability of nitrogen (N) is one of the factors that controls the productivity of the oceans, and there has been great interest in determining the magnitudes and pathways of N inputs to the world's oceans through biological N2 fixation (Glossary). Biological N2 fixation is the reduction of N2 gas to biologically available ammonium, and this is performed by a diverse but limited number of bacterial and archaeal genera. Cyanobacteria are generally assumed to be the major N2-fixing
Oceanic N2-fixing cyanobacteria
There are diverse cyanobacteria in terrestrial and aquatic ecosystems that can fix N2, and these habitats span extremes from high to low temperatures [3]. Thus, the open ocean N2-fixing cyanobacteria in theory could include diverse taxa of differing morphologies, and a longstanding research question has been why are there not more N2-fixing microorganisms in the low-nutrient regions of the open ocean? With the exception of the filamentous heterocyst-forming cyanobacteria, it is impossible to
Trichodesmium
Although data on other N2-fixing cyanobacteria are sparse, the most abundant N2-fixing microorganism in the open ocean is probably the filamentous non-heterocyst-forming cyanobacterium Trichodesmium 13, 14. Trichodesmium is a filamentous cyanobacterium that often forms colonies or aggregates, known as ‘puffs’ and ‘tufts’. These aggregates are easily observed and collected and are the reason why other groups of cyanobacteria did not previously receive much attention. However, even Trichodesmium
Heterocyst-forming cyanobacteria
In estuaries and the Baltic Sea, common N2-fixing cyanobacterial blooms are composed of heterocyst-forming cyanobacteria, but these groups of N2-fixing cyanobacteria are not extremely abundant in oligotrophic oceans. The reasons for the lack of heterocyst-forming species in the oceans have been addressed by several hypotheses, including sensitivity to turbulence [23]. More recently, detailed modeling of oxygen solubility and diffusion coefficients in warm seawater has indicated that the
Unicellular cyanobacteria
The cyanobacterial nifH genes found in open ocean water samples (first at Station ALOHA in the North Pacific Ocean) cluster into two groups (termed ‘group A’ or UCYN-A, and ‘group A’ or UCYN-B) [4]. A nifH gene identified as unicellular ‘group C’ (i.e. UCYN-C) was subsequently reported from the North Atlantic 9, 11, 35, 36, and is most similar to the nifH of the benthic Cyanothece and some diatom endosymbionts (Figure 1). The group B nifH sequence is essentially identical to that from a
Physiology of N2-fixing cyanobacteria
Cyanobacteria are primarily oxygenic phototrophs and have light-driven daily cycles that control metabolism. The major oceanic N2-fixing cyanobacteria have distinct daily patterns (Table 1). Unicellular cyanobacteria such as Crocosphaera fix N2 during the dark phase, presumably to avoid O2 inactivation of nitrogenase. Conversely, heterocyst-forming cyanobacteria such as the symbionts of diatoms, fix N2 during the day (Table 1). Trichodesmium fixes N2 during the day. The patterns of N2 fixation
Biogeography of N2 fixation and N2-fixing cyanobacteria
From biological and ecosystem perspectives it is crucial to understand how N2-fixing cyanobacteria are spatially distributed. Previously, geographical constraints upon N2 fixation were hypothesized from the known distributions of Trichodesmium, or from the temperature range believed to constrain growth and N2 fixation in Trichodesmium. Knowledge of the factors that constrain growth can be used for the development of models to predict the distributions of different groups of diazotrophs [71].
Concluding remarks
Open ocean N2-fixing cyanobacteria continue to provide surprises in ecology, biology and physiology. The marine nonheterocyst-forming cyanobacterium Trichodesmium appears to be the most abundant N2-fixing cyanobacterium, although the mechanisms of aerobic N2 fixation in this cyanobacterium are not yet well understood. New information on the genetics and physiology of cyanobacterial symbionts of diatoms is being obtained using nanoSIMS and genomics, but the mechanisms of symbiont interactions
Acknowledgments
I would like to thank Kendra Turk, Shellie Bench, Jim Tripp, Mary Hogan, and Rachel Foster for their many contributions to this review. Mary Margaret Perez helped with preparation of the manuscript. I would like to also thank Doug Capone (University of Southern California), Robert Hamersley (Soka University), Ian Hewson (Cornell), Margaret Mulholland (Old Dominion University), David Scanlan (Warwick) and Andy Rees (Plymouth Marine Laboratory) [Atlantic Meridional Transect consortium
Glossary
- Denitrification
- the reduction of oxidized forms of N, including nitrate and nitrite, to N2 gas, resulting in loss of biologically-available N from the ecosystem. Denitrification is a respiratory process in some Bacteria and Archaea.
- Diatoms
- single-celled eukaryotic algae of the Bacillariophyta that have a silica frustule. These are common algae in phytoplankton. Some diatoms harbor N2-fixing cyanobacteria.
- Diazotroph
- a N2-fixing microorganism. Diazotrophs are composed of some Bacteria (including
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