Richelia

Richelia
Scientific classification
Domain: Bacteria
Phylum: Cyanobacteria
Class: Cyanophyceae
Order: Nostocales
Family: Nostocaceae
Genus: Richelia
J.Schmidt
Species:
R. intracellularis
Binomial name
Richelia intracellularis
C.H.Ostenfeld ex J.Schmidt, 1901

Richelia is a genus of nitrogen-fixing filamentous heterocystous 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.

Morphology

Richelia are made up of filaments called trichomes, which are fine hair-like structures that grow out of a myriad of plant species, though their presence as free-living organisms in the marine environment is rare.[1][2] The number of trichomes Richelia have in each diatom host varies.[3] The trichomes serve the purpose of nitrogen fixation as well as nutrient exchange with host diatoms.[2] The location of Richelia within their various diatom symbionts is not fully known, though it is commonly assumed to be within the diatom’s periplasmic space between the plasmalemma and the frustule.[4][5]  Richelia’s trichomes are made up of two cell types: Heterocyst and Vegetative. The heterocyst is a terminal single cell within which nitrogen fixation occurs, while the rest of the trichome is made up of vegetative cells within which photosynthesis occurs.[2] Some Richelia are made up of many vegetative cells and a terminal heterocyst, while others only contain a terminal heterocyst.[3] The heterocyst is characterized by a thick glycolipid layer which minimizes oxygen's ability to interfere with nitrogen fixation.[2] This is important to Richelia’s function as oxygen can bind to nitrogenase and inhibit the cyanobacteria's nitrogen fixing abilities.[2] The heterocyst does not divide, while the vegetative cells do.[2]  Richelia also remain photosynthetically active while within their host diatoms, a behaviour that is somewhat uncommon for similar symbionts.[2]

Symbiosis

Nitrogen fixation and symbiosis

Nitrogen fixation is an important biological process in marine ecosystems. In many regions of the world's oceans the availability of inorganic nitrogen such as nitrate and ammonium limits the rate of photosynthesis (primary productivity). Hence, organisms that form symbiotic relationships with other organisms, often cyanobacteria, to fix nitrogen can be at an advantage. In many cyanobacteria, nitrogen fixation is carried out in specialized cells called heterocysts. Cyanobacteria in the genus Richelia are an example of cyanobacteria are capable of fixing nitrogen gas into organic forms of nitrogen.[6] The organic nitrogen can then be transferred from the cyanobacteria to the diatoms with which they have a symbiotic relationship.[6] Evidence of this nitrogen transfer has been observed multiple times, and this relationship has benefits for both the Richelia cells, which exist inside the diatom, and the diatom itself. For example, the growth of cyanobacteria inside the diatom is increased, releasing carbon dioxide through respiration that can be used by the diatom in photosynthesis. The diatom benefits from enhanced growth as a result of the nitrogen fixed by the cyanobacteria.[1] The presence of this symbiosis can allow diatoms to persist through nitrogen limiting conditions.[1]

Host specificity

Richelia's host specificity and location within a host has been linked to the symbiont genome evolution. Even for taxonomically and morphologically related organisms, preference for diatom hosts and locations within a host differ.[7] These differences usually depend on which host a symbiont typically resides in. For example, in the Hemiaulus and Richelia symbiosis, Richelia resides inside the siliceous frustule of Hemiaulus. Richelia lacks principal nitrogen metabolism enzymes and transporters, such as ammonium transporters, nitrate and nitrite reductases as well as glutamate synthase. It also has a reduced genome, likely following the genome streamlining theory. Hemiaulus has genes that code for all of these enzymes and transporters while lacking the nitrogen fixation genes present in Richelia. This allows the host to complement its symbiont and vice versa, resulting in host specificity that follows host and symbiont genome evolution.[7]

Coordination of gene expression

Day-night cycles potentially play a role in coordination of resource exchange and cell division between a diazotroph and its diatom host. Photosynthesis, nitrogen fixation, and resource acquisition related genes show day-night fluctuations in their expression pattern in Richelia. Nitrogen uptake, metabolism, and carbon transport gene expression in diatom hosts seem to be synchronized with nitrogen fixation gene expression in Richelia, suggesting a coordinated exchange of nitrogen and carbon. Symbiont-host cell physiology is thought to be coordinated and strongly dependent on each other, especially with regard to the time of the day.[8]

Species associations

While studies have identified Richelia in up to 13 species, there is a debate as to how many of those identifications were accurate.[9]

The diatom-Richelia symbiotic relationships that are confirmed and most well-known are as follows:

  • Rhizosolenia (Diatom)-Richelia symbiosis which occurs inside the Diatom cell. It is located outside the plasma membrane in the periplasmic space[10][11]
  • Hemiaulus (Diatom)-Richelia symbiosis which also happens inside the Diatom cell. The exact location is currently unknown.[11] Hemiaulus-Richelia symbiosis is often associated with Trichodesmium, especially in transitional waters.[12]
  • Another form of symbiosis was found between ChaetocerosChaetoceros (Diatom) and Richelia, but it appears to be rare.[13]

Life cycle

Within diatom hosts

Richelia are most commonly found and best understood within host diatoms. For most of its life cycle within diatoms, the orientation of Richelia cells remains unchanged[14] with the orientation of the terminal heterocyst cell fixed towards the closest diatom valve.[4][14] This orientation only changes during separation and migration of the Richelia trichomes.[14] This separation and migration is presumed to occur synchronously with growth and division of the host diatom as it produces daughter cells, in order to provide new daughter cells with symbionts. While transfer of the Richelia trichome to daughter cells can occur before division, this method will eventually end as it limits vegetative growth due to the progressive reduction in the size of the host diatom. Within diatoms that are dead or dying, some Richelia cells have enlarged and rounded vegetative cells, some begin to disintegrate and die with their host, and some emerge from a trichome-shaped opening in the diatom frustule and presumably become free-living Richelia .[4]

Free-living

While Richelia cells can exist as free-living organisms in the marine environment, it is rarely observed. Additionally, how diatoms without symbionts are colonized by free-living Richelia is unknown; however, a number of mechanisms have been hypothesized, including Richelia cells entering non-colonized diatoms directly. Also hypothesized is that Richelia cells may be affiliated with auxospore cells, or may enter diatoms during sexual reproduction when the trichome is transported to the auxospore. Richelia cells may also colonize diatoms during instances of vegetative cell enlargement.[4]

Distribution

Cyanobacteria in the genus Richelia are primarily found in symbiotic association with diatoms in nitrogen-limited regions of the ocean.[2] This distribution pattern is attributed to the symbiotic relationship that Richelia forms with different species of diatoms in which they provide diatoms with nitrogen that is otherwise limiting for growth.[2] Similar to other diazotrophs, Richelia cells are in low abundances in productive equatorial regions due to nutrient upwelling and in high abundances in non-productive subtropical areas where low concentrations of nitrate limit the growth of diatoms.[15]

Quantitative analyses of the distribution of Richelia is an emerging field of study.[15] Thus far, many observations have been subject to criticism due to issues of misidentifying hosts and the associated diazotrophs, and demonstrating symbiotic relationships overall.[16]

Global ocean

Richelia are found throughout the Pacific Ocean, the Atlantic Ocean, the Amazon River plume, and the Mediterranean Sea.[15][17] They follow similar distributions to other diazotrophs including cyanobacteria in the genus Trichodesmium, Candidatus Atelocyanobacterium thalassa (formerly known as UCYN-A), and UCYN-B, which are in high abundance throughout much of the tropical oceans, although the relative abundances of the different taxa varies.[15] The abundance of Richelia cells also varies based on different environmental conditions across regions.[15] Richelia, when compared to other diazotrophs, show lower abundances at deeper depths.[15] Warm, silicate-rich conditions, such as those found in the Amazon River plume, allow for high Richelia growth rates.[15] Richelia cells also decrease in abundance as inorganic nitrogen increases because they are at a competitive disadvantage when nitrate concentrations are high.[15] However, unlike other diazotrophs, Richelia cells do not decrease in abundance when phosphate levels are high.[15] THe abundances of Richelia cells also depend on the availability of iron, due to the iron requirements of the enzyme nitrogenase that is needed to fix di-nitrogen gas.[15] Grazing is also a factor that may affect the abundances of diazotrophs throughout different regions in the global ocean.[18]

Mediterranean Sea

Richelia is an endosymbiont with diatoms such as Rhizosolenia spp. and Hemiaulus spp.[17] Richelia is found to be highly correlated with the presence of Hemiaulus spp., and sporadically correlated with the presence of Rhizosolenia spp.[17] The highest counts of Richelia as sampled in 2006 in the Eastern Mediterranean Sea are 50 heterocysts L−1 in June and October in coastal regions, and 50 heterocysts L−1 in June and November in pelagic regions.[17] These peaks occur during a deepening of the mixed layer depth at each region.[17] Richelia and Hemiaulus hauckii are found together in both coastal and pelagic regions year-round in diurnal and nocturnal sampling, and it is suggested that this symbiotic pair has an evolutionary advantage over other host options for Richelia.[3][17] Because the Eastern Mediterranean Sea has oligotrophic conditions due to a large transport of nutrients out to the North Atlantic Ocean through the Strait of Gibraltar, Richelia provides important nitrogen fixation capabilities for diatoms they form symbiotic relationships with. Free living Richelia are not considered to be present in the Eastern Mediterranean Sea based on the current sampling experiment results available. In the Eastern Mediterranean Sea water columns, Richelia is the primary diurnal organism with an expression of the nifH gene. A case of allopatric speciation is observed between coastal and pelagic water columns in the Eastern Mediterranean Sea. These two regions have different clades of nifH-expressing cells of Richelia, hypothesized to be due to the restriction of the two regions from each other by a hydrological barrier caused by the sloping of the continental shelf.[17]

Western/Southwestern Pacific Ocean

Richelia have been found as epiphytes to Chaetoceros compressus and to Rhizosolenia clevei in the Western Pacific Ocean. It is hypothesized that Richelia filaments can detach from Rhizosolenia clevei and subsequently become symbionts to Chaetoceros compressus. This is suggested as the Richelia and Chaetoceros compressus symbiosis has been found to follow occurrences of the Richelia and Rhizosolenia clevei symbiosis.[16]

Kuroshio Current

The distribution of Richelia in the Kuroshio Current varies based on the section of the current and the time of year. Physical and hydrographical conditions vary throughout the year in the current and create changes to the growth of bacterial and diatom colonies. Conditions in May limit growth to a more narrow region of the current than in July. The region has low concentrations of nitrate throughout both Spring and Summer, with July seeing the least nitrate levels in surface waters. The number of Richelia filaments per colony of Chaetoceros compressus ranges from 4 to 9 during May to November, reaching a maximum in July. The maximum abundance of the Richelia and Chaetoceros compressus symbiosis occurs in July, at 10 colonies L−1. The maximum abundance of the Richelia and Rhizosolenia clevei symbiosis also occurs in July, at 30 colonies L−1.

Sulu Sea

Symbiosis between Richelia and Chaetoceros compressus has also been observed in the Southern Sulu Sea. This is due to the lower than 0.1 μM nitrogen concentrations in surface waters causing nitrogen limiting conditions.[16]

Indian Ocean

Richelia have been found as epiphytes to Chaetoceros compressus in the Indian Ocean.[16]

Western Tropical Atlantic Ocean

Nitrogen fixation and cyanobacteria-diatom symbiosis occur in the freshwater layer of the Amazon River plume due to low surface nitrate conditions. In these nitrogen limited areas, Richelia can be found in symbiosis with Rhizosolenia clevei and Hemiaulus spp. Richelia symbiosis with H. hauckii is found predominantly in this region with depth as well as throughout the surface. The abundance of the symbiosis between Richelia and H. hauckii is higher further northwest from the Amazon River outflow. A positive correlation can be found between salinity and abundances of Richelia symbioses.[16]

References

  1. 1 2 3 Foster RA, Kuypers MM, Vagner T, Paerl RW, Musat N, Zehr JP (September 2011). "Nitrogen fixation and transfer in open ocean diatom-cyanobacterial symbioses". The ISME Journal. 5 (9): 1484–93. doi:10.1038/ismej.2011.26. PMC 3160684. PMID 21451586.
  2. 1 2 3 4 5 6 7 8 9 Inomura K, Follett CL, Masuda T, Eichner M, Prášil O, Deutsch C (February 2020). "Carbon Transfer from the Host Diatom Enables Fast Growth and High Rate of N2 Fixation by Symbiotic Heterocystous Cyanobacteria". Plants. 9 (2): 192. doi:10.3390/plants9020192. PMC 7076409. PMID 32033207.
  3. 1 2 3 Foster RA, Subramaniam A, Mahaffey C, Carpenter EJ, Capone DG, Zehr JP (March 2007). "Influence of the Amazon River plume on distributions of free-living and symbiotic cyanobacteria in the western tropical north Atlantic Ocean". Limnology and Oceanography. 52 (2): 517–532. Bibcode:2007LimOc..52..517F. doi:10.4319/lo.2007.52.2.0517.
  4. 1 2 3 4 Villareal TA (December 1989). "Division cycles in the nitrogen-fixing Rhizosolenia (Bacillariophyceae)-Richelia (Nostocaceae) symbiosis". British Phycological Journal. 24 (4): 357–365. doi:10.1080/00071618900650371.
  5. ↑ Caputo A, Nylander JA, Foster RA (January 2019). "The genetic diversity and evolution of diatom-diazotroph associations highlights traits favoring symbiont integration". FEMS Microbiology Letters. 366 (2). doi:10.1093/femsle/fny297. PMC 6341774. PMID 30629176.
  6. 1 2 Bonnet S, Berthelot H, Turk-Kubo K, Cornet-Barthaux V, Fawcett S, Berman-Frank I, et al. (2016). "Diazotroph derived nitrogen supports diatom growth in the South West Pacific: A quantitative study using nanoSIMS". Limnology and Oceanography. 61 (5): 1549–1562. Bibcode:2016LimOc..61.1549B. doi:10.1002/lno.10300. JSTOR 26628504.
  7. 1 2 Hilton JA, Foster RA, Tripp HJ, Carter BJ, Zehr JP, Villareal TA (2013-04-23). "Genomic deletions disrupt nitrogen metabolism pathways of a cyanobacterial diatom symbiont". Nature Communications. 4 (1): 1767. Bibcode:2013NatCo...4.1767H. doi:10.1038/ncomms2748. PMC 3667715. PMID 23612308.
  8. ↑ Harke MJ, Frischkorn KR, Haley ST, Aylward FO, Zehr JP, Dyhrman ST (January 2019). "Periodic and coordinated gene expression between a diazotroph and its diatom host". The ISME Journal. 13 (1): 118–131. doi:10.1038/s41396-018-0262-2. PMC 6299110. PMID 30116042.
  9. ↑ Foster RA, O'Mullan GD (2008-01-01). "Chapter 27 - Nitrogen-Fixing and Nitrifying Symbioses in the Marine Environment". In Capone DG, Bronk DA, Mulholland MR, Carpenter EJ (eds.). Nitrogen in the Marine Environment (Second ed.). San Diego: Academic Press. pp. 1197–1218. doi:10.1016/b978-0-12-372522-6.00027-x. ISBN 978-0-12-372522-6.
  10. ↑ Villareal TA (1992). "Marine Nitrogen-Fixing Diatom-Cyanobacteria Symbioses". In Carpenter EJ, Capone DG, Rueter JG (eds.). Marine Pelagic Cyanobacteria: Trichodesmium and other Diazotrophs. NATO ASI Series. Dordrecht: Springer Netherlands. pp. 163–175. doi:10.1007/978-94-015-7977-3_10. ISBN 978-94-015-7977-3.
  11. 1 2 Pyle AE, Johnson AM, Villareal TA (2020-10-08). "Isolation, growth, and nitrogen fixation rates of the Hemiaulus-Richelia (diatom-cyanobacterium) symbiosis in culture". PeerJ. 8: e10115. doi:10.7717/peerj.10115. PMC 7548074. PMID 33083143.
  12. ↑ Carpenter EJ, Montoya JP, Burns J, Mulholland MR, Subramaniam A, Capone DG (1999). "Extensive bloom of a N2-fixing diatom/cyanobacterial association in the tropical Atlantic Ocean". Marine Ecology Progress Series. 185: 273–283. Bibcode:1999MEPS..185..273C. doi:10.3354/meps185273. ISSN 0171-8630.
  13. ↑ Janson S, Wouters J, Bergman B, Carpenter EJ (October 1999). "Host specificity in the Richelia-diatom symbiosis revealed by hetR gene sequence analysis". Environmental Microbiology. 1 (5): 431–8. doi:10.1046/j.1462-2920.1999.00053.x. PMID 11207763.
  14. 1 2 3 Villareal TA (June 1990). "Laboratory Culture and Preliminary Characterization of the Nitrogen-Fixing Rhizosolenia-Richelia Symbiosis". Marine Ecology. 11 (2): 117–132. Bibcode:1990MarEc..11..117V. doi:10.1111/j.1439-0485.1990.tb00233.x.
  15. 1 2 3 4 5 6 7 8 9 10 Tang W, Cassar N (2019). "Data-Driven Modeling of the Distribution of Diazotrophs in the Global Ocean" (PDF). Geophysical Research Letters. 46 (21): 12258–12269. Bibcode:2019GeoRL..4612258T. doi:10.1029/2019GL084376. ISSN 1944-8007.
  16. 1 2 3 4 5 Gómez F, Furuya KE, Takeda S (2005-04-01). "Distribution of the cyanobacterium Richelia intracellularis as an epiphyte of the diatom Chaetoceros compressus in the western Pacific Ocean". Journal of Plankton Research. 27 (4): 323–330. doi:10.1093/plankt/fbi007.
  17. 1 2 3 4 5 6 7 Zeev EB, Yogev T, Man-Aharonovich D, Kress N, Herut B, Béjà O, Berman-Frank I (September 2008). "Seasonal dynamics of the endosymbiotic, nitrogen-fixing cyanobacterium Richelia intracellularis in the eastern Mediterranean Sea". The ISME Journal. 2 (9): 911–23. doi:10.1038/ismej.2008.56. PMID 18580972. S2CID 205156514.
  18. ↑ Wang WL, Moore JK, Martiny AC, Primeau FW (February 2019). "Convergent estimates of marine nitrogen fixation". Nature. 566 (7743): 205–211. Bibcode:2019Natur.566..205W. doi:10.1038/s41586-019-0911-2. PMID 30760914. S2CID 61156495.
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