Trichodesmium erythraeum

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Trichodesmium erythraeum
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Bacteria
Phylum: Cyanobacteria
Class: Cyanophyceae
Order: Oscillatoriales
Family: Microcoleaceae
Genus: Trichodesmium
Species:
T. erythraeum
Binomial name
Trichodesmium erythraeum
Ehrenburg ex Gomont

Trichodesmium erythraeum is a marine cyanobacteria species characterized by its prolific diazotrophic capabilities. [1] They play a dominant role in the ocean ecosystem, supplying a steady and significant source of new, biologically available nitrogen and cycling phosphorus. [2] By nature of its filamentous morphology, T. erythraeum is also known to congregate into large, long colonies, sizeable enough to be seen as sawdust-like particles to the naked eye and pigmented marine regions in satellite images, typically found in oligotrophic tropical and subtropical waters. [3] These blooms are responsible for the famous coloration of the Red Sea. [4]

Contents

Etymology/nomenclature

The genus name is inspired from the ancient Greek roots: “Tricho-” meaning  ‘hair’ [5] and “-desmós”, meaning band or connection. [6] The species name erythraeum is also derived from the Greek “Eruthraî” or the related latin term “Erythraeus” which means red or reddish. [7] The historical Greek root is also used in Erythrà Thálassa, which translates to and is known as the Red Sea or the Erythraean Sea. [7]

History

Discovery

The Trichodesmium genus was first described by James Cook in 1770 while traveling along the subtropical coast of Australia. [8] Charles Darwin had also reportedly recorded the unique Trichodesmium blooms while on his famous voyage on the Beagle , describing it as “sea sawdust”. [3] Christian Gottfried Ehrenberg named this particular species -  Trichodesmium erythraeum - in 1830 as he was traveling across the Red Sea during a period of red bloom. [4] In the following century, other scientists on seafaring expeditions would come to name other Trichodesmium species such as T. thiebautti, T. hildebrandtii, and T. contortum. [4] While there is still uncertainty about their taxonomy and phylogenetic relationships, T. erythraeum is the most well-studied species as well as the only one whose genome has been sequenced within the genus. [4]

Isolation/methods

Trichodesmium erythraeum was first isolated and sequenced in 1991 from the Atlantic coast of North Carolina. [8] Researchers Prufert-Debout, Pearl, and Lassen modified seawater medium with 0.1 N HCl and 0.1 N NaOH to reach a basic pH of 8.17, then tested for growth of individual algal cells in variations of the culture medium. [9] In order to further isolate the Trichodesmium, they added cycloheximide, effectively killing eukaryotic microbial colonies. They maintained sterile growth media, closely monitoring then measuring the growth and formation of bacterial aggregates. [9] The Trichodesmium cultures were incubated on a light-dark cycle at 24 °C atop a shake table to simulate tidal movement. [9] This experiment yielded various morphological arrangements of aggregated T. erythraeum IMS101 filaments. [9] [10]

Morphology

Trichodesmium erythraeum is a motile, Gram-negative cyanobacteria. [11] They can exist in single filaments, but are more commonly found in colonial morphologies composed of up to several hundreds of filaments. [12] Generally, Trichodesmium can aggregate in parallel to form a fusiform (tuft) colony or radial (puff) form. [12] [13] The defining characteristic of T. erythraeum is its pigment composition, containing chlorophyll A and phycoerythrin. [14] Phycoerythrin is a photosynthetic pigment that causes T. erythraeum to reflect its eponymous rusty red color. [1] [14] At least 50% of the T. erythraeum cell is occupied by large gas-filled vacuoles which aid in buoyancy and alignment with other cells in colonial formation. [1] [15]

Genomics

Trichodesmium erythraeum is the sole Trichodesmium species with a fully sequenced genome, and it remains one of the larger cyanobacterial genomes currently sequenced, at around 7.75 Mbp in length. [16] Among 58 cyanobacterial genomes, phylogenetic analysis indicates T. erythraeum is closely related to the genera Lyngbya , inhabitants of marine waters, and Arthrospira, primarily found in more alkaline lakes, as part of a larger lineage made up of filamentous non-heterocystous species within the order Oscillatoriales . [16] Though T. erythraeum is non-heterocystous, recent findings in comparative genomics support relatedness to heterocystous cyanobacteria genera. [16]

The genus Trichodesmium encompasses 5 other species apart from T. erythraeum, characterized and differentiated by cell and colony morphology, pigmentation, and buoyancy. [17] These 5 species were originally organized into two different clades, categorized according to the cellular arrangement and consequent regulation of buoyancy, as well as their glycogen clusters, which facilitate carbon storage. [16] In one clade, there was T. erythraeum and T. tenue, while the other clade held T. thiebautti, T. hildebrandtii, and T. contortum. [16] However, recent genomic analysis aimed at species differentiation revealed three distinct clades, reorganizing the six species as follows: 1) T. thiebautti, T. hildebrandtii, 2) T. contortum, T. tenue, and 3) T. erythraeum. [18]

Physiology

Trichodesmium erythraeum plays an important role in aquatic microenvironments, specifically in warm and nutrient-scarce oceans, where its diazotrophic metabolism contributes a substantial amount of fixed nitrogen (~50% of total N from all six Trichodesmium species) to these ecosystems. [10] One of the defining features of T. erythraeum is its ability to conduct nitrogen fixation and carbon sequestration simultaneously without forming heterocysts, as opposed to other cyanobacterial species capable of these processes. [9]  

Metabolism

For non-heterocystous N2-fixing cyanobacteria, metabolism is normally defined by two specialized separation strategies: N2 fixation occurring at night and photosynthesis during the light of day. [19] Interestingly, Trichodesmium performs both oxygenic photosynthesis and atmospheric nitrogen fixation exclusively during the day, attributed to 1) enhanced O2 consumption during peak nitrogenase activity and 2) conglomeration of the O2-sensitive nitrogenase enzyme complexes within "diazocytes," or localized sets of cells within the filamentous colony. [19] While T. erythraeum can carry out these processes simultaneously, studies have shown that photosynthesis and nitrogen fixation may follow a circadian rhythm. [20] In addition, nitrogen fixation by T. erythraeum depends on the availability of inorganic phosphorus and iron, as nutrient limitation may inhibit population growth. [10] In particular, the Trichodesmium IMS101 genome has protein-encoding genes that are advantageous for growth in oligotrophic, low-phosphate environments. [21] The orientation of T. erythraeum in its environment can directly affect it's metabolic activity. Specifically, Trichodesmium blooms generally occur at ocean surface where they can access atmospheric nitrogen for diazotrophy; however, sub-surface colonies are also occasionally observed, likely utilizing dissolved nitrogen or other nitrogen sources from the ocean depths. [14]

Ecology

Trichodesmium blooms are integral to marine ecosystems because of their nitrogen fixation capabilities, uptake of phosphorus, and supply of substrates that in turn provision of shelter for marine life. [22] These blooms depend on several factors: warm oceans, high salt content, and a steady supply of light and nutrients (Fe and P, specifically). [22] One bloom, recorded in the Arabian Sea, coincided with increased bioavailability of trace metals, highlighting their importance in Trichodesmium metabolism, as well as the ecological implications of these blooms. [23]

Significance and applications

Recent reports of unprecedented T. erythraeum blooms in the Mediterranean, [24] Andaman, [25] and Arabian [26] Seas underscore the toxic nature and potential harmful effects of these blooms. In the Andaman Sea, an increase in water temperature and an upsurge in salinity resulted in lower rates of hooking fish, [25] while increases in pH and decreased oxygen availability led to greater fish mortality in the Arabian Sea. [26] As global warming persists, changes in the temperature and marine composition of traditional Trichodesmium habitats may induce a greater frequency of blooms. Ocean acidification has also stimulated increased production of reactive oxygen species (ROS) and exopolysaccharides (EPS) by T. erythraeum [27] which may further aggravate environmental imbalance. Under ordinary circumstances, T. erythraeum blooms confer many benefits to marine ecosystems, however irregular and frequent blooms coinciding with ongoing climate change may prove detrimental to these environments in the long run.

Related Research Articles

Nitrogen fixation is a chemical process by which molecular nitrogen (N
2), which has a strong triple covalent bond, is converted into ammonia (NH
3) or related nitrogenous compounds, typically in soil or aquatic systems but also in industry. The nitrogen in air is molecular dinitrogen, a relatively nonreactive molecule that is metabolically useless to all but a few microorganisms. Biological nitrogen fixation or diazotrophy is an important microbe-mediated process that converts dinitrogen (N2) gas to ammonia (NH3) using the nitrogenase protein complex (Nif).

<span class="mw-page-title-main">Cyanobacteria</span> Phylum of photosynthesising prokaryotes that can produce toxic blooms in lakes and other waters

Cyanobacteria, also called Cyanobacteriota or Cyanophyta, are a phylum of autotrophic gram-negative bacteria that can obtain biological energy via photosynthesis. The name 'cyanobacteria' refers to their color, which similarly forms the basis of cyanobacteria's common name, blue-green algae, although they are not scientifically classified as algae. They appear to have originated in a freshwater or terrestrial environment.

<i>Prochlorococcus</i> Genus of bacteria

Prochlorococcus is a genus of very small (0.6 μm) marine cyanobacteria with an unusual pigmentation. These bacteria belong to the photosynthetic picoplankton and are probably the most abundant photosynthetic organism on Earth. Prochlorococcus microbes are among the major primary producers in the ocean, responsible for a large percentage of the photosynthetic production of oxygen. Prochlorococcus strains, called ecotypes, have physiological differences enabling them to exploit different ecological niches. Analysis of the genome sequences of Prochlorococcus strains show that 1,273 genes are common to all strains, and the average genome size is about 2,000 genes. In contrast, eukaryotic algae have over 10,000 genes.

<i>Trichodesmium</i> Genus of bacteria

Trichodesmium, also called sea sawdust, is a genus of filamentous cyanobacteria. They are found in nutrient poor tropical and subtropical ocean waters. Trichodesmium is a diazotroph; that is, it fixes atmospheric nitrogen into ammonium, a nutrient used by other organisms. Trichodesmium is thought to fix nitrogen on such a scale that it accounts for almost half of the nitrogen fixation in marine systems globally. Trichodesmium is the only known diazotroph able to fix nitrogen in daylight under aerobic conditions without the use of heterocysts.

Diazotrophs are bacteria and archaea that fix atmospheric nitrogen(N2) in the atmosphere into bioavailable forms such as ammonia.

<i>Aphanizomenon flos-aquae</i> Species of bacterium

Aphanizomenon flos-aquae is a brackish and freshwater species of cyanobacteria of the genus Aphanizomenon found around the world, including the Baltic Sea and the Great Lakes.

<i>Synechococcus</i> Genus of bacteria

Synechococcus is a unicellular cyanobacterium that is very widespread in the marine environment. Its size varies from 0.8 to 1.5 µm. The photosynthetic coccoid cells are preferentially found in well–lit surface waters where it can be very abundant. Many freshwater species of Synechococcus have also been described.

<span class="mw-page-title-main">Cyanophage</span> Virus that infects cyanobacteria

Cyanophages are viruses that infect cyanobacteria, also known as Cyanophyta or blue-green algae. Cyanobacteria are a phylum of bacteria that obtain their energy through the process of photosynthesis. Although cyanobacteria metabolize photoautotrophically like eukaryotic plants, they have prokaryotic cell structure. Cyanophages can be found in both freshwater and marine environments. Marine and freshwater cyanophages have icosahedral heads, which contain double-stranded DNA, attached to a tail by connector proteins. The size of the head and tail vary among species of cyanophages. Cyanophages infect a wide range of cyanobacteria and are key regulators of the cyanobacterial populations in aquatic environments, and may aid in the prevention of cyanobacterial blooms in freshwater and marine ecosystems. These blooms can pose a danger to humans and other animals, particularly in eutrophic freshwater lakes. Infection by these viruses is highly prevalent in cells belonging to Synechococcus spp. in marine environments, where up to 5% of cells belonging to marine cyanobacterial cells have been reported to contain mature phage particles.

<i>Aphanizomenon</i> Genus of bacteria

Aphanizomenon is a genus of cyanobacteria that inhabits freshwater lakes and can cause dense blooms. They are unicellular organisms that consolidate into linear (non-branching) chains called trichomes. Parallel trichomes can then further unite into aggregates called rafts. Cyanobacteria such as Aphanizomenon are known for using photosynthesis to create energy and therefore use sunlight as their energy source. Aphanizomenon bacteria also play a big role in the Nitrogen cycle since they can perform nitrogen fixation. Studies on the species Aphanizomenon flos-aquae have shown that it can regulate buoyancy through light-induced changes in turgor pressure. It is also able to move by means of gliding, though the specific mechanism by which this is possible is not yet known.

Cyanobionts are cyanobacteria that live in symbiosis with a wide range of organisms such as terrestrial or aquatic plants; as well as, algal and fungal species. They can reside within extracellular or intracellular structures of the host. In order for a cyanobacterium to successfully form a symbiotic relationship, it must be able to exchange signals with the host, overcome defense mounted by the host, be capable of hormogonia formation, chemotaxis, heterocyst formation, as well as possess adequate resilience to reside in host tissue which may present extreme conditions, such as low oxygen levels, and/or acidic mucilage. The most well-known plant-associated cyanobionts belong to the genus Nostoc. With the ability to differentiate into several cell types that have various functions, members of the genus Nostoc have the morphological plasticity, flexibility and adaptability to adjust to a wide range of environmental conditions, contributing to its high capacity to form symbiotic relationships with other organisms. Several cyanobionts involved with fungi and marine organisms also belong to the genera Richelia, Calothrix, Synechocystis, Aphanocapsa and Anabaena, as well as the species Oscillatoria spongeliae. Although there are many documented symbioses between cyanobacteria and marine organisms, little is known about the nature of many of these symbioses. The possibility of discovering more novel symbiotic relationships is apparent from preliminary microscopic observations.

<span class="mw-page-title-main">Bacterioplankton</span> Bacterial component of the plankton that drifts in the water column

Bacterioplankton refers to the bacterial component of the plankton that drifts in the water column. The name comes from the Ancient Greek word πλανκτος, meaning "wanderer" or "drifter", and bacterium, a Latin term coined in the 19th century by Christian Gottfried Ehrenberg. They are found in both seawater and freshwater.

CandidatusAtelocyanobacterium thalassa, also referred to as UCYN-A, is a diazotrophic species of cyanobacteria commonly found in measurable quantities throughout the world's oceans and some seas. Members of A. thalassa are spheroid in shape and are 1-2 μm in diameter, and provide nitrogen to ocean regions by fixing non biologically available atmospheric nitrogen into biologically available ammonium that other marine microorganisms can use.

Anabaena variabilis is a species of filamentous cyanobacterium. This species of the genus Anabaena and the domain Eubacteria is capable of photosynthesis. This species is heterotrophic, meaning that it may grow without light in the presence of fructose. It also can convert atmospheric dinitrogen to ammonia via nitrogen fixation.

Raphidiopsis raciborskii is a freshwater cyanobacterium.

<i>Cyanothece</i> Genus of bacteria

Cyanothece is a genus of unicellular, diazotrophic, oxygenic photosynthesizing cyanobacteria.

<i>Crocosphaera watsonii</i> Species of bacterium

Crocosphaera watsonii is an isolate of a species of unicellular diazotrophic marine cyanobacteria which represent less than 0.1% of the marine microbial population. They thrive in offshore, open-ocean oligotrophic regions where the waters are warmer than 24 degrees Celsius. Crocosphaera watsonii cell density can exceed 1,000 cells per milliliter within the euphotic zone; however, their growth may be limited by the concentration of phosphorus. Crocosphaera watsonii are able to contribute to the oceanic carbon and nitrogen budgets in tropical oceans due to their size, abundance, and rapid growth rate. Crocosphaera watsonii are unicellular nitrogen fixers that fix atmospheric nitrogen to ammonia during the night and contribute to new nitrogen in the oceans. They are a major source of nitrogen to open-ocean systems. Nitrogen fixation is important in the oceans as it not only allows phytoplankton to continue growing when nitrogen and ammonium are in very low supply but it also replenishes other forms of nitrogen, thus fertilizing the ocean and allowing more phytoplankton growth.

Trichodesmium thiebautii is a cyanobacteria that is often found in open oceans of tropical and subtropical regions and is known to be a contributor to large oceanic surface blooms. This microbial species is a diazotroph, meaning it fixes nitrogen gas (N2), but it does so without the use of heterocysts. T. thiebautii is able to simultaneously perform oxygenic photosynthesis. T. thiebautii was discovered in 1892 by M.A. Gomont. T. thiebautii are important for nutrient cycling in marine habitats because of their ability to fix N2, a limiting nutrient in ocean ecosystems.

<i>Oscillatoria brevis</i> Species of bacterium

Oscillatoria brevis is a species of the genus Oscillatoria first identified in 1892. It is a blue-green filamentous cyanobacterium, which can be found in brackish and fresh waterways. O. brevis can also be isolated from soil.

<span class="mw-page-title-main">Marine prokaryotes</span> Marine bacteria and marine archaea

Marine prokaryotes are marine bacteria and marine archaea. They are defined by their habitat as prokaryotes that live in marine environments, that is, in the saltwater of seas or oceans or the brackish water of coastal estuaries. All cellular life forms can be divided into prokaryotes and eukaryotes. Eukaryotes are organisms whose cells have a nucleus enclosed within membranes, whereas prokaryotes are the organisms that do not have a nucleus enclosed within a membrane. The three-domain system of classifying life adds another division: the prokaryotes are divided into two domains of life, the microscopic bacteria and the microscopic archaea, while everything else, the eukaryotes, become the third domain.

Richelia is a genus of nitrogen-fixing, filamentous, heterocystous and cyanobacteria. It contains the single species Richelia intracellularis. They exist as both free-living organisms as well as symbionts within potentially up to 13 diatoms distributed throughout the global ocean. As a symbiont, Richelia can associate epiphytically and as endosymbionts within the periplasmic space between the cell membrane and cell wall of diatoms.

References

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  2. ↑ Fu, Fei-Xue; Zhang, Yaohong; Bell, Peter R. F.; Hutchins, David A. (2005). "PHOSPHATE UPTAKE AND GROWTH KINETICS OF TRICHODESMIUM (CYANOBACTERIA) ISOLATES FROM THE NORTH ATLANTIC OCEAN AND THE GREAT BARRIER REEF, AUSTRALIA1". Journal of Phycology. 41 (1): 62–73. doi:10.1111/j.1529-8817.2005.04063.x. ISSN   0022-3646.
  3. 1 2 "Sea Sawdust off Gladstone". earthobservatory.nasa.gov. 2017-10-07. Retrieved 2024-04-17.
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  5. ↑ "tricho-", Wiktionary, the free dictionary, 2023-03-17, retrieved 2024-04-27
  6. ↑ "Desmos", Wiktionary, the free dictionary, 2024-03-24, retrieved 2024-04-27
  7. 1 2 "Erythraean", Wiktionary, the free dictionary, 2023-01-17, retrieved 2024-04-27
  8. 1 2 Orcutt, K. M.; Rasmussen, U.; Webb, E. A.; Waterbury, J. B.; Gundersen, K.; Bergman, B. (2002). "Characterization of Trichodesmium spp. by Genetic Techniques". Applied and Environmental Microbiology. 68 (5): 2236–2245. doi:10.1128/AEM.68.5.2236-2245.2002. ISSN   0099-2240. PMC   127538 . PMID   11976093.
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  11. ↑ Inomura, Keisuke; Wilson, Samuel T.; Deutsch, Curtis (2019-08-27). Gilbert, Jack (ed.). "Mechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine Trichodesmium". mSystems. 4 (4). doi:10.1128/mSystems.00210-19. ISSN   2379-5077. PMC   6687940 . PMID   31387928.
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  13. ↑ Wang, Siyuan; Koedooder, Coco; Zhang, Futing; Kessler, Nivi; Eichner, Meri; Shi, Dalin; Shaked, Yeala (2022). "Colonies of the marine cyanobacterium Trichodesmium optimize dust utilization by selective collection and retention of nutrient-rich particles". iScience. 25 (1): 103587. doi:10.1016/j.isci.2021.103587. PMC   8718973 . PMID   35005537.
  14. 1 2 3 Boatman, Tobias G.; Davey, Phillip A.; Lawson, Tracy; Geider, Richard J. (2018-04-11). Campbell, Douglas A. (ed.). "The physiological cost of diazotrophy for Trichodesmium erythraeum IMS101". PLOS ONE. 13 (4): e0195638. doi: 10.1371/journal.pone.0195638 . ISSN   1932-6203. PMC   5895029 . PMID   29641568.
  15. ↑ Baalen, Chase; Brown, R. Malcolm (1969). "The ultrastructure of the marine blue green alga, Trichodesmium erythraeum, with special reference to the cell wall, gas vacuoles, and cylindrical bodies". Archiv für Mikrobiologie. 69 (1): 79–91. doi:10.1007/BF00408566. ISSN   0302-8933. PMID   4986297.
  16. 1 2 3 4 5 Bergman, Birgitta; Sandh, Gustaf; Lin, Senjie; Larsson, John; Carpenter, Edward J. (May 2013). "Trichodesmium – a widespread marine cyanobacterium with unusual nitrogen fixation properties". FEMS Microbiology Reviews. 37 (3): 286–302. doi:10.1111/j.1574-6976.2012.00352.x. ISSN   1574-6976. PMC   3655545 . PMID   22928644.
  17. ↑ "Home - Trichodesmium erythraeum IMS101". genome.jgi.doe.gov. Retrieved 2024-04-03.
  18. ↑ Orcutt, K. M.; Rasmussen, U.; Webb, E. A.; Waterbury, J. B.; Gundersen, K.; Bergman, B. (May 2002). "Characterization of Trichodesmium spp. by Genetic Techniques". Applied and Environmental Microbiology. 68 (5): 2236–2245. doi:10.1128/AEM.68.5.2236-2245.2002. ISSN   0099-2240. PMC   127538 . PMID   11976093.
  19. 1 2 Sandh, Gustaf; Ran, Liang; Xu, Linghua; Sundqvist, Gustav; Bulone, Vincent; Bergman, Birgitta (January 2011). "Comparative proteomic profiles of the marine cyanobacterium Trichodesmium erythraeum IMS101 under different nitrogen regimes". Proteomics. 11 (3): 406–419. doi:10.1002/pmic.201000382. ISSN   1615-9853. PMID   21268270 – via Wiley Analytical Science.
  20. ↑ Cai, Xiaoni; Gao, Kunshan (2015-08-10). Chauvat, Franck (ed.). "Levels of Daily Light Doses Under Changed Day-Night Cycles Regulate Temporal Segregation of Photosynthesis and N2 Fixation in the Cyanobacterium Trichodesmium erythraeum IMS101". PLOS ONE. 10 (8): e0135401. doi: 10.1371/journal.pone.0135401 . ISSN   1932-6203. PMC   4530936 . PMID   26258473.
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  23. ↑ Krishnan, Anoop A.; Krishnakumar, P.K.; Rajagopalan, M. (February 2007). "Trichodesmium erythraeum (Ehrenberg) bloom along the southwest coast of India (Arabian Sea) and its impact on trace metal concentrations in seawater". Estuarine, Coastal and Shelf Science. 71 (3–4): 641–646. doi:10.1016/j.ecss.2006.09.012 – via Elsevier Science Direct.
  24. ↑ Spatharis, Sofie; Skliris, Nikolaos; Meziti, Alexandra; Kormas, Konstantinos (March 2012). Weyhenmeyer, Gesa (ed.). "First record of a Trichodesmium erythraeum bloom in the Mediterranean Sea". Canadian Journal of Fisheries and Aquatic Sciences. 69 (8): 1444–1455. doi:10.1139/f2012-020. ISSN   0706-652X – via ResearchGate.
  25. 1 2 Kumar, Arun; Padmavati, Gadi; Pradeep, Hosahalli (2015-06-15). "Occurrence of Trichodesmium Erythraeum (Cyanophyte) Bloom and Its Effects on the Fish Catch during April 2013, in the Andaman Sea". Applied Environmental Research: 49–57. doi: 10.35762/AER.2015.37.2.4 . ISSN   2287-075X.
  26. 1 2 Al Busaidi, Saud S.; Al Rashdi, Khalfan M.; Al Gheilani, Hamed M.; Amer, Shehla (2008-01-01). "Hydrographical Observations during a Red Tide with Fish Mortalities at Masirah Island, Oman". Journal of Agricultural and Marine Sciences [JAMS]. 13: 64. doi:10.24200/jams.vol13iss0pp64-72. ISSN   2410-1079.
  27. ↑ Wu, Shijie; Mi, Tiezhu; Zhen, Yu; Yu, Kaiqiang; Wang, Fuwen; Yu, Zhigang (September 2020). "A Rise in ROS and EPS Production: New Insights into the Trichodesmium erythraeum Response to Ocean Acidification". Journal of Phycology. 57 (1): 172–182. doi:10.1111/jpy.13075. ISSN   0022-3646. PMID   32975309 – via Wiley Online Library.
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