Trichodesmium erythraeum

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A Microbial Biorealm page on the genus Trichodesmium erythraeum

Classification

Higher order taxa

Bacteria; Cyanobacteria; Oscillatoriales; Trichodesmium; Trichodesmium erythraeum http://www.ncbi.nlm.nih.gov/Taxonomy/Browser

Species

Trichodesmium erythraeum

Description and significance

Trichodesmium is a genus of cyanobacteria that is found in tropical and subtropical ocean waters with low nutrient levels. Trichodesmium erythraeum is a species of the Trichodesmium genus that occurs as filaments of 20-200 cells. These filaments often congregate with Trichodesmium thiebautii to form larger colonies called blooms that can be seen by the naked eye (Karl 2002). Because Trichodesmium is able to form such large structures, it has been observed in oceans long before being isolated in laboratories. In fact, the first documented observation of Trichodesmium was made in 1770 by Captain Cook on a voyage in the Coral Sea near Australia. It is known as "sea-sawdust" and accumulations of large blooms can lead to discoloration of the water and "red tides" (Hallegraef 1995). This genus is of great interest because it has been found to contribute over 40% of all nitrogen fixation that occurs in the ocean. In addition, there has been evidence that Trichodesmium blooms can have a toxic effect on invertebrates and humans (see Pathology).

Genome structure

The complete genome of Trichodesmium erythraeum has been sequenced by the Joint Genome Institute. It contains 7,750,108 base pairs that comprise a single circular chromosome(http://expasy.org). Analysis of the genome has shown that 63.83% of the total 775 kilobases code for DNA and that the G-C content of the genome is about 34% (http://img.jgi.doe.gov). Sequences coding for nitrogenase in T. erythraeum show 98% homology with those found in Trichodesmium thiebautii. This high level of sequence conservation between species may be indicative of the central role that nitrogenase in the process of nitrogen fixation in both species. Trichodesmium is thought to have branched off from other cyanobacteria early in its evolution because of a low level (about 75%) of similarity with other cyanobacteria with sequenced genomes, but 16S rDNA sequence analysis of the genome suggest that T. erythraeum is closely related to bacteria of the genus Oscillatoria (Capone 1997). T. erythraeum is not known to contain any plasmids.

Cell structure and metabolism

Trichodesumium erythraeum contain gas vesicles which can occupy up to 60-70% of the total cell volume. Within the cell, these gas vacuoles are aligned so that their longitudinal axis is oriented perpendicular to the direction of the filament(Van Baalen 1969). These gas vesicles allow T. erythraeum an amount of buoyancy according to changes in the concentration of carbohydrates within the cell (Capone 1997). Photosynthetic lamallae can be seen throughout the cell, but tend to be more populous toward the center of the cell (Van Baalen 1969).

Two major metabolic processes take place in T. erythraeum: carbon fixation and nitrogen fixation. Like other cyanobacteria, T. erythraeum are able to derive energy through the process of photosynthesis. Photosynthesis serves to drive carbon fixation in the cells and leads to the production of organic carbon in the form of sugar, oxygen and energy in the form of ATP. In the process of nitrogen fixation, T. erythraeum convert inorganic nitrogen gas to organic forms of organic nitrogen that can be utilized by other organisms. Since nitrogenase, an enzyme needed for nitrogen fixation, is inactivated in the presence of oxygen, nitrogen fixing bacteria have developed ways to protect the nitrogenase within them from oxygen. Trichodesmium are thought to do this by keeping nitrogenase and oxygen physically separated in a manner not unlike the compartmentalization of oxygen demonstrated by heterocystous cyanobacteria (Bergman 1991). During times of high nitrogen fixation researcher have observed an increase in photosynthetically inactive areas in Trichodesmium colonies. This suggests that in addition to spatial separation, nitrogenase is segregated from oxygen in time by downregulating the amount of photosynthetically derived oxygen when nitrogenase activites are at their highest (Bergman 2001).

Ecology

Trichodesmium erythraeum lives in tropical and subtropical areas of oceans and tend be most populous in shallow waters above 40 meters in depth (Capone 1997). This species is important to the global ecosystem because it contributes upwards of 40% of all nitrogen fixation occurring in the ocean (Karl 2002). Often T. erythraeum cells combine with cells T. thiebautii cells to form large blooms that span thousands of square kilometers (Karl 2002). As discussed in the "Pathology" section of this page, these blooms have been found to have toxic effects on both marine invertebrates and humans. The mechanism by which toxicity occurs is still unclear as toxicity has not been clearly tied to a specific substrate. Large Trichodesmium blooms have been found to contain "a microcosm including bacteria, other cyanobacteria, protozoa, fungi, hydrozoans, and copepods" and are thought to serve as a source of carbon and nitrogen for such organisms (Capone 1997;p 1224). In addition, expansive Trichodesmium blooms are thought to affect the amount of light that is able to reach lower levels of water and the ability of gases and heat to be exchanged between the air and the ocean. Although Trichodesmium blooms are a good source of newly fixed carbon and nitrogen, they serve as a food source only for a selected group of copepods because others organisms are deterred by a toxin produced by the blooms (Capone 1997).

Pathology

The large Trichodesmium blooms formed of T. thiebautii and T. erythraeum have been connected to toxicity in marine invertebrates as well as humans. While isolates of T. erythraeum cells were not found to be toxic to mice, except at high concentrations (500g/kg mouse), they have been linked to the mortality of various marine organisms (Hawser 1992, Guo 1992). In humans, Trichodesmium blooms have been associated with a respiratory syndrome known as Tamandare or Trichodesmium fever (Sudek 2006). Currently no known toxin has been succesfully isolated from Trichodesmium erythraeum. Chemical assays of lipophilic T. erythraeum from Australia have not been able to detect common neurotoxins, but it is possible that different strains of bacteria as well as different environmental factors may lead to a difference in the development of toxins in T. erythraeum (Negri 2003).

In addition, T. erythraeum can cause harm to other organisms through a variety of mechanisms besides toxin production. When blossoms of this cyanobacteria decay, they cause the surrounding environnment to become anoxic. The low oxygen conditions resulting from bloom decay has been associated with the death of pearl oysters at a farm in India as well as the death of shrimp and fish in a farm in Thailand (Chellham 1978, Suvavpun 1989). It is also a possibility that T. erythraeum can cause harm to nearby organisms by promoting the formation of blooms of other species that may produce toxins or have a harmful effect(Sudek 2006).

Application to Biotechnology

While Trichodesmium erythraeum contributes to surrounding ecosystems by its fixation of carbon and nitrogen, it has not yet been utilized widely in biotechnology, a variety of uses have been found for other cyanobacteria. For instance, marine cyanobacteria have been experimentally determined to be a good food source for Tilapia fish and other animal models, and therefore have potential to be useful in the development of feed for various organisms. Scientists have also found uses for cyanobacteria as fertilizers, in waste treatment, and for the commercial production of enzymes and pharmaceuticals (Thajjudin 2005).

As more research is conducted on T. erythraeum it is likely that scientists will be able to discover potential uses in biotechnology. It is unlikely that T. erythraeum would be useful as feed for marine organisms, as it is suspected to produce harmful toxins and there are not many organisms that use it as a primary food source in its natural habitat. However, it is likely that this species could produce an enzyme or toxin that may prove useful to humans in medicine and research.

Current Research

Phosphonate utilization by the globally important marine diazotroph Trichodesmium (Dyhrman 2006)

Trichodesmium erythraeum are able to utilize about 75% of the dissolved organic phosphate (DOP) in their ocean environment. This study proposes that Trichodesmium erythraeum is also able to use phosphonate (the remaining 25% of the DOP) as a source of phosphorous in metabolic processes. Analysis of the T. erythraeum genome has shown that the organism possesses orthologs of phn genes that are responsible for phosphonate transport and a C-P lyase complex in the cell membrane in other species of bacteria. These cellular components are important in C-P lyase pathways that allow the breaking of carbon-phosphate ester bonds to free phosphate for use in the cell. The presence of such orthologs in all species of Trichodesmium that have been tested suggests that these features arised early in the evolution of the genus. The similarity of phn orthologs in Trichodesmium to genes in Thiobacillus as well as their increased GC content in comparison to the rest of the Trichodesmium genome are evidence that they were incorporated by horizontal gene transfer. mRNA analysis of T. erythraeum samples from the Sargasso Sea show that phn genes are expressed only when cells experience low levels of phosphorous cycling. This ability of T. erythraeum to regulate gene expression suggests that this bacteria is indeed able to utilize phosphonate as a source of phosphorous through a C-P lyase pathway when other phosphorous sources are limited. This ability could convey an advantage to T. erythraeum and help explain the high abundance of this cyanobacteria in ocean environments with limited nutrients.

Structure of trichamide, a cyclic peptide from the bloom-forming cyanobacterium Trichodesmium erythraeum, predicted from the genome sequence (Sudek 2006) Researchers have discovered a 12.5kb gene cluster in Trichodesmium erythraeum that has a similar sequence to the pat gene cluster in another cyanobacteria called Prochloron didemni. The pat gene codes for a cyclic proteins called patellamides that have been shown to have a mild cytotoxicity. The gene cluster in T. erythraeum was named the tri cluster and its product, trichamide, is predicted to be cytotoxic. The information that is known about the pat cluster and patellamides were used to predict the structure and biosynthetic pathway for trichamide. Experiments demonstrated the trichamide is a hydrophilic molecule localized within the cell and not excreted to the outside environment in large amounts. From this information, researchers predict that trichamide may serve as a type of defense to deter organisms from consuming I>T. erythraeum cells. The lack of trichamide excretion in healthy cells also supports the evidence of cytotoxic effects in marine organisms induced by decaying or lysed I>T. erythraeum but not normal cells. The continued development of DNA technology and sequencing databases provides an array of opportunity for the discovery of many previously uncharacterized cell products and components.

Overexpression and characterization of an iron storage and DNA-binding Dps protein from Trichodesmium erythraeum (Castruita 2006) Although iron is important to the process of nitrogen fixation in cyanobacteria, iron storage proteins have not yet been isolated from marine microorganisms. This study marks the first identification of an iron storage protein, a Dps (DNA binding protein) in Trichodesmium erythraeum. Analysis of the amino acid sequence of T. erythraeumIM101 revealed two genes that appear to have a significant amount of homology with genes known to code for bacterioferritin (iron storage protein) components. These genes demonstrated conservation of sequences important for iron binding cores. The Dps protein isolated from T. erythraeum was able to bind Iron and incorporate phosphate, both characteristics of other members of the ferritin family. In addition, the Dps isolated was able to bind DNA with a much higher affinity than Dps proteins from E. coli. When DNA incubated with Dps were exposed to DNase I they were not degraded, which provides evidence that in addition to serving as an iron storage protein, Dps in T. erythraeum help DNA from damage. This proctection against DNA damage may especially important for T. erythraeum because their exposure to UV light and execution of metabolic processes provides oxidative stress which could prove harmful to the organism.

References

Bergman, B., and E. J. Carpenter. Nitrogenase confined to randomly distributed trichomes in the marine cyanobacterium Trichodesmium thiebautii. 1991. J. Phycol. 27:158-165.

Berman-Frank, I., P. Lundgren, Y.-B. Chen, H. Kupper, Z. Kolber, B. Bergman, and P. Falkowski. Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. 2001. Science 294:1534-1537.

Capone,D., J. Zehr, H. Paerl, B. Berman, E. Carpenter. Trichodesmium, a globally significant marine cyanobacterium. 1997. Science 276:1221-1229. http://www.sciencemag.org

Castruita M, Saito M, Schottel PC, Elmegreen LA, Myneni S, Stiefel EI, Morel FM. Overexpression and characterization of an iron storage and DNA-binding Dps protein from Trichodesmium erythraeum. Appl Environ Microbiol. 2006 Apr;72(4):2918-24. http://www.pubmedcentral.nih.gov/picrender.fcgi?artid=1449065&blobtype=pdf

Chellham, A., Alagarswami, K. Blooms of Trichodesmium thiebautii and their effects on experimental pearl culture in the Pambau area and its effect on the fauna. 1978. Curr. Sci. 10, 263.

Dyhrman, S., et al. Phosphonate utilization by the globally important marine diazotroph Trichodesmium. 2006. Nature 439(7072):68-71. http://www.nature.com/nature/journal/v439/n7072/abs/nature04203.html;jsessionid=2404FD5D585CEF00B47C677BCBC28B85

ExPAsy database http://expasy.org/sprot/hamap/TRIEI.html

Guo, C., and P. A. Tester. Toxic effect of the bloom-forming Trichodesmium sp. (cyanophyta) to the copepod Acartia tonsa. 1994. Nat. Toxins 2:222-227. http://www.ncbi.nlm.nih.gov/sites/entrez?Db=pubmed&Cmd=ShowDetailView&TermToSearch=7952947&ordinalpos=4&itool=EntrezSystem2.PEntrez.Pubmed.Pubmed_ResultsPanel.Pubmed_RVDocSum

Hallegraeff, G. Marine phytoplankton communities in the Australian region: current status and the future threats. 1995. State of the Marine Environment Report for Australia: The Marine Environment - Technical Annex: 1 http://www.environment.gov.au/coasts/publications/somer/annex1/phytoplankton.html

Hawser, S. P., J. M. O'Neil, M. R. Roman, and G. A. Codd. Toxicity of blooms of the cyanobacterium Trichodesmium to zooplankton. 1992. J. Appl. Phycol. 4:79-86.

Karl, D., A. Michaels, B. Bergman, D. Capone, E. Carpenter, R. Letelier, F. Lipschultz, H. Paerl, D. Sigman, and L. Stal. Dinitrogen fixation in the world’s oceans. 2002. Biogeochemistry 57–58:47–98.

NCBI database http://www.ncbi.nlm.nih.gov/Taxonomy/Browser

Negri, A., O. Bunter, B. Jones, L. Llewllyn. Effects of the bloom-forming alga Trichodesmium erythraeum on the pearl oyster Pinctada maxima. 2003. Aquaculture:91-102.

Sudek S, Haygood MG, Youssef DT, Schmidt EW. Structure of trichamide, a cyclic peptide from the bloom-forming cyanobacterium Trichodesmium erythraeum, predicted from the genome sequence. 2006. Appl Environ Microbiol. 2006 Jun;72(6):4382-7. http://www.pubmedcentral.nih.gov/picrender.fcgi?artid=1489667&blobtype=pdf

Suvapepun, S. Occurrences of red tide in the Gulf of Thailand. In: Okaichi, T., Anderson, D.M., Nemoto, T. (Eds.), International Symposium on Red Tides, Takamatsu (Japan), 10– 14 Nov 1987, Red Tides: Biology, Environmental Science and Toxicology. 1989. Elsevier, New York, pp. 41– 44.

Thajuddin, S., G. Subramanian. Cyanobacterial biodiversity and potential applications in biotechnology. 2005. Current Science, 89(1):47-57. http://www.ias.ac.in/currsci/jul102005/47.pdf

Van Baalen C, Brown RM Jr. The ultrastructure of the marine blue green alga, Trichodesmium erythraeum, with special reference to the cell wall, gas vacuoles, and cylindrical bodies. 1969. Arch Mikrobiol. 69(1):79-91.

Edited by Tara Tsukamoto student of Rachel Larsen and Kit Pogliano

KMG