ALL Metrics
-
Views
-
Downloads
Get PDF
Get XML
Cite
Export
Track
Review

The cyanobacterial nitrogen fixation paradox in natural waters

[version 1; peer review: 2 approved]
PUBLISHED 09 Mar 2017
Author details Author details
OPEN PEER REVIEW
REVIEWER STATUS

Abstract

Nitrogen fixation, the enzymatic conversion of atmospheric N (N2) to ammonia (NH3), is a microbially mediated process by which “new” N is supplied to N-deficient water bodies. Certain bloom-forming cyanobacterial species are capable of conducting N2 fixation; hence, they are able to circumvent N limitation in these waters. However, this anaerobic process is highly sensitive to oxygen, and since cyanobacteria produce oxygen in photosynthesis, they are faced with a paradoxical situation, where one critically important (for supporting growth) biochemical process is inhibited by another.

N2-fixing cyanobacterial taxa have developed an array of biochemical, morphological, and ecological adaptations to minimize the “oxygen problem”; however, none of these allows N2 fixation to function at a high enough efficiency so that it can supply N needs at the ecosystem scale, where N losses via denitrification, burial, and advection often exceed the inputs of “new” N by N2 fixation. As a result, most marine and freshwater ecosystems exhibit chronic N limitation of primary production. Under conditions of perpetual N limitation, external inputs of N from human sources (agricultural, urban, and industrial) play a central role in determining ecosystem fertility and, in the case of N overenrichment, excessive primary production or eutrophication. This points to the importance of controlling external N inputs (in addition to traditional phosphorus controls) as a means of ensuring acceptable water quality and safe water supplies.

Nitrogen fixation, the enzymatic conversion of atmospheric N2 to ammonia (NH3) is a  microbially-mediated process by which “new” nitrogen is supplied to N-deficient water bodies.  Certain bloom-forming cyanobacterial species are capable of conducting N2 fixation; hence they are able to circumvent nitrogen limitation in these waters. However, this anaerobic process is highly sensitive to oxygen, and since cyanobacteria produce oxygen in photosynthesis, they are faced with a paradoxical situation, where one critically-important (for supporting growth) biochemical process is inhibited by another. Diazotrophic cyanobacterial taxa have developed an array of biochemical, morphological and ecological adaptations to minimize the “oxygen problem”; however, none of these allows N2 fixation to function at a high enough efficiency so that it can supply N needs at the ecosystem scale, where N losses via denitrification, burial and advection often exceed the inputs of “new” N by N2 fixation. 

As a result, most marine and freshwater ecosystems exhibit chronic N-limitation of primary production.  Under conditions of perpetual N limitation, external inputs of N from human sources (agricultural, urban, industrial) play a central role in determining ecosystem fertility and in the case of N-overenrichment, excessive primary production, or eutrophication. This points to the importance of controlling external N inputs (in addition to traditional phosphorus controls) as a means of ensuring acceptable water quality and safe water supplies.    

Keywords

cyanobacteria, nitrogen fixation, freshwater, marine

Nitrogen fixation, the biochemical conversion of “inert” atmospheric N (N2) to biologically available ammonia (NH3), is a microbially mediated process of global significance because it provides “new” N to aquatic ecosystems in which biological production is often controlled by N availability1,2. N2 fixation is an anaerobic process carried out by specific prokaryotes, including heterotrophic and chemolithotrophic bacteria and some cyanobacteria (blue-green algae)3. The process likely evolved during the oxygen (O2)-devoid Precambrian period some 2+ billion years ago4,5. Of the N2-fixing microbial taxa, the cyanobacteria are of particular biogeochemical and ecological interest because they were also the first O2-evolving photosynthetic organisms on Earth6; their proliferation during this period is thought to be an evolutionary “milestone” because it led to the generation of an O2-rich atmosphere, a prerequisite for the evolution of O2-requiring fungi, bacteria, animals, and higher plant species on our planet6.

Ironically, the development of an O2-rich atmosphere, hydrosphere, and pedosphere constituted a formidable biochemical challenge for the cyanobacteria because, while they were capable of fixing N2, the process had to be confined to an O2-free micro-environment7. This requirement posed a serious dilemma, especially for aquatic cyanobacteria, because they require illuminated conditions in surface waters, but the high ambient O2 levels produced by photosynthesis in these waters also represents an environmental barrier to O2-sensitive N2 fixation. Over their long evolutionary history, cyanobacteria have developed biochemical and structural adaptations as well as biotic associations in order to optimize N2 fixation while relying on oxygenic photosynthesis to provide energy and organic carbon (C) compounds to support metabolism and growth. The adaptions include (1) confining N2 fixation to night-time when photosynthesis is “turned off”, (2) forming colonies and aggregates to reduce illumination and form low-O2 “microzones”, (3) participating as endosymbionts in biological associations, and (4), forming heterocysts (non-photosynthetic, O2-free cells) in some filamentous taxa, which allows N2 fixation to proceed while receiving photo-reductant and organic C through photosynthesis from adjacent cells8.

These are all remarkably clever adaptations to a modern-day oxic biosphere, which help circumvent the “O2 problem”6. From an ecosystem perspective, they have allowed N2-fixing species to provide biologically available N from the vast reservoir of atmospheric N2. However, on the ecosystem scale, recent N budget analyses indicate that N2 fixation inputs fall far short of meeting ecosystem requirements when biologically available N inputs (from terrestrial and atmospheric sources) and losses (via denitrification, sedimentation and burial, and advection) are considered911. As a result, freshwater, estuarine, and marine systems are often chronically N deficient1117. Pervasive N limitation has many implications for ecosystem function, especially when excessive external nutrient inputs lead to accelerating primary production (eutrophication), harmful algal blooms, and excessive O2 consumption (hypoxia). If chronic N-limited conditions prevail in water bodies and N2 fixation cannot meet ecosystem N requirements, then external N inputs often supply N to support eutrophication and its unwanted symptoms. From a management perspective, this means that the growing global glut of N inputs from agricultural, urban, and industrial sources14,1820 needs to be controlled, in addition to the broadly accepted phosphorus (P) input constraints, in order to protect our waterways and water supplies.

Why does N2 fixation fall short of meeting ecosystem demands? Apparently, this process does not operate at sufficient rates in a modern-day, oxic world to compensate for losses via burial, export, and denitrification, even though it is protected and optimized by the various biological adaptations mentioned above. It is counteracted at larger scales by biogeochemical processes, such as denitrification, that run in the opposite direction (NO3 → N2). The N2-fixing process is an energy-demanding one, requiring 16 ATP molecules to fix one molecule of N23. In cyanobacteria, this energy demand has to be met by photosynthesis, while in non-photosynthetic bacteria, organic matter and redox reactions serve as energy sources3. In highly productive (eutrophic), turbid waters where cyanobacteria and bacteria thrive, the availability of photosynthetically active radiation (PAR: 400–700 nm) is often restricted, causing a radiant energy deficit and suboptimal N2 fixation rates. Secondly, cyanobacteria taxa that dominate in eutrophic waters often accumulate as thick surface “blooms”, in part to circumvent light limitation in subsurface waters11. High rates of photosynthesis in such blooms lead to O2 supersaturation, often in excess of 200% saturation21. These ambient O2 levels inhibit N2 fixation in situ, even in heterocystous taxa22,23. Thirdly, N2 fixation requires high levels of P (to support the energetics, e.g. ATP formation and nucleic acid production) and metals, most prominently iron (Fe), which is a co-factor in the enzyme complex nitrogenase3. In highly oxygenated surface waters, Fe occurs as the insoluble and biologically unavailable Fe3+ ion that may lead to Fe-limited conditions24. Lastly, wind-induced turbulence and vertical mixing can reduce N2 fixation potential by disrupting colonies and aggregates and enhancing inward diffusion of O2 (Figure 1)25 and deepening the mixed layer, reducing light availability.

c01bc943-4fc9-46da-9318-3b10d1d22cd9_figure1.gif

Figure 1. The nitrogen fixing process, as mediated by cyanobacteria (utilizing oxygenic photosynthesis as an energy and carbon source) as well as heterotrophic and chemolithotrophic microorganisms, in eutrophic surface waters.

Potential environmental controls, including phosphorus (P) and iron (Fe) availability, energy sources, and dissolved oxygen inhibition, are shown in red. The background photo is of an O2-supersaturated (during daytime) cyanobacterial surface bloom in Lake Taihu, China. Photograph by H. Paerl.

Thus, while N2 fixation converts inert N2 into biologically available NH3 to support aquatic fertility in a remarkable fashion, it faces multiple constraints and limitations in aquatic environments, especially in surface waters, which are often N limited. Geochemists, some limnologists, and a few oceanographers have assumed that as long as P and Fe are readily available, N2 fixation should make up for an N deficit, given the unlimited supply of N2 available26,27. However, this assumed linear stoichiometric relationship is not straightforward. Major environmental factors constrain this process, preventing it from functioning at optimal rates and supplying complete ecosystem N requirements8,11. As a result, much of the world’s marine and freshwater environments remain chronically N deficient. In practical (management) terms, this limitation means that external inputs of N play a key role in providing adequate and excessive fertility (eutrophication) of many freshwater and most marine ecosystems11,15,16. Tremendous increases in anthropogenically generated bioavailable N in the form of synthetic (Haber process) fertilizers, agricultural, industrial, and urban wastes, and N2 emissions (as both oxides and reduced forms of N) far overshadow biological fixation of N2 in providing available N to receiving waters. Effective future management and protection of our fresh and marine waters will depend on the control of external inputs of both N and P11,27 instead of depending on the more traditional approach of controlling P inputs without N restrictions28.

Comments on this article Comments (0)

Version 1
VERSION 1 PUBLISHED 09 Mar 2017
Comment
Author details Author details
Competing interests
Grant information
Copyright
Download
 
Export To
metrics
Views Downloads
F1000Research - -
PubMed Central
Data from PMC are received and updated monthly.
- -
Citations
CITE
how to cite this article
Paerl H. The cyanobacterial nitrogen fixation paradox in natural waters [version 1; peer review: 2 approved]. F1000Research 2017, 6(F1000 Faculty Rev):244 (https://doi.org/10.12688/f1000research.10603.1)
NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article.
track
receive updates on this article
Track an article to receive email alerts on any updates to this article.

Open Peer Review

Current Reviewer Status: ?
Key to Reviewer Statuses VIEW
ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions
Version 1
VERSION 1
PUBLISHED 09 Mar 2017
Views
0
Cite
Reviewer Report 09 Mar 2017
James Cotner, University of Minnesota, St. Paul, MN, 55108, USA 
Approved
VIEWS 0
I confirm that I have read this submission and believe that I have an ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Cotner J. Reviewer Report For: The cyanobacterial nitrogen fixation paradox in natural waters [version 1; peer review: 2 approved]. F1000Research 2017, 6(F1000 Faculty Rev):244 (https://doi.org/10.5256/f1000research.11426.r20665)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
Views
0
Cite
Reviewer Report 09 Mar 2017
Justin Chaffin, Stone Laboratory, Ohio State University, Put-in-Bay, OH, USA 
Approved
VIEWS 0
I confirm that I have read this submission and believe that I have an ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Chaffin J. Reviewer Report For: The cyanobacterial nitrogen fixation paradox in natural waters [version 1; peer review: 2 approved]. F1000Research 2017, 6(F1000 Faculty Rev):244 (https://doi.org/10.5256/f1000research.11426.r20666)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.

Comments on this article Comments (0)

Version 1
VERSION 1 PUBLISHED 09 Mar 2017
Comment
Alongside their report, reviewers assign a status to the article:
Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
Sign In
If you've forgotten your password, please enter your email address below and we'll send you instructions on how to reset your password.

The email address should be the one you originally registered with F1000.

Email address not valid, please try again

You registered with F1000 via Google, so we cannot reset your password.

To sign in, please click here.

If you still need help with your Google account password, please click here.

You registered with F1000 via Facebook, so we cannot reset your password.

To sign in, please click here.

If you still need help with your Facebook account password, please click here.

Code not correct, please try again
Email us for further assistance.
Server error, please try again.