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Skeletonema costatum

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Skeletonema costatum
Scientific classification Edit this classification
Domain: Eukaryota
Clade: Diaphoretickes
Clade: SAR
Clade: Stramenopiles
Phylum: Gyrista
Subphylum: Ochrophytina
Class: Bacillariophyceae
Order: Thalassiosirales
Family: Skeletonemataceae
Genus: Skeletonema
Species:
S. costatum
Binomial name
Skeletonema costatum
(Greville) Cleve, 1866

Skeletonema costatum is a cosmopolitan centric diatom that belongs to the genus Skeletonema.[1] It was first described by R. K. Greville, who originally named it Melosira costata, in 1866.[1] It was later renamed by Cleve in 1873[2] and was more narrowly defined by Zingone et al.[3] and Sarno et al.[4][5] S. costatum is the most well known species of Skeletonema and is often one of the dominant species responsible for red tide events.[4][6][7]

S. costatum is known for its carbon acquisition mechanisms[8][9][10][11], and has been used in the production of biofuel[12][13][14][15] and as a feed for aquaculture[16][17][18]. S. costatum is appealing for commercial use due to its high photosynthetic efficiency[13][15], high tolerance to pH, temperature, and salinity changes[19][14], high lipid and fatty acid content[20][12][14][15][20], and rapid growth rate.[13][21][22]

Structure and morphology

A single chain of Skeletonema costatum cells from a field sample from Long Island Sound

S. costatum is a single-celled organism that exists on average in long chains of 6 to 24 cells[23] but can be up to 60 cells.[3] As with all diatoms, the siliceous cell wall (the frustule) consists of two interlocking components ("like two halves of a petri dish"[24]), the hypotheca and epitheca[25]. Each cell is approximately 8 to 12 μm in diameter[5] and about 3.5 to 11.5 μm apart from each other.[23][5] The cells are connected by long straight fultoportula processes[26] and contain up to 2 chloroplasts per cell.[23] Processes are tube-like silicified projections that protrude from the valve wall.[25] A fultoportula processes (also known as strutted processes) protrude through the valve wall with 2 or mote satellite pores surrounding them.[24][25] Fultoportula processes are only found in the centric order Thalassiosirales.[24] S. costatum have 3 satellite pores per fultoportula process and terminal fultoportulae processes with claw-like tips.[5]

S. costatum have cylindrically shaped cells and a ring of long flattened intercalary fultoportula processes protruding from the periphery of each valve, each closed along their entire length.[3] Each intercalary fultoportula has a longitudinal suture extending from an external pore at its base to its tip.[5]

Intercalary fultoportula processes of adjacent valves are connected at a 1:2 junction, where each intercalary fultoportula process interlocks with two intercalary fultoportula processes, creating a "zigzag appearance".[5] This 1:2 junction is a distinctive feature of S. costatum.[5] Their intercalary rimoportula are positioned marginally, they have long terminal rimoportula, and their cingular band features rows of pores.[5] Each valve has one of their fultoportulae replaced with a rimoportula, identified by its longer external process and the "spoutlike teapot" shaped tip of the terminal rimoportulae.[5]

Morphologically similar species

Among the Skeletonema species, S. costatum is most morphologically similar to S. subsalsum, both exhibiting rows of small pores between the parallel rows of transverse branching ribs on their girdle bands.[5] They are also the only two Skeletonema species with long intercalary rimoportula processes.[5] S. costatum can be identified by the persistent presence of a 1:2 junction, and the closed tubules of its intercalary fultoportulae processes[5]. S. subsalsum will sometimes have a 1:1 junction.[5]

Morphological variation

The morphological plasticity of S. costatum has been extensively studied.[27][28][29][23] Castillo (1995) attributes significant variations in morphological features, such as cell diameter, the number of cells per chain and the length of intercalary processes, with variations in environmental conditions, most notably, salinity.[23] If cultured in freshwater, S. costatum develops short intercellular processes,[30] and at 1 psu, are observed with seemingly no space between sibling valves.[5]

Taxonomy

As of 2021, 21 Skeletonema species were "identified and taxonomically accepted", Skeletonema costatum being one of them.[31]

S. costatum was first described by R. K. Greville in 1866, originally called Melosira costata,[1] and later renamed by Cleve in 1873.[2] S. costatum has since been more narrowly defined, with numerous species previously attributed to S. costatum identified as distinct species.[3][32][4][5]

The species originally described by Greville in 1866 is often referred to as S. costatum sensu lato (s. l.),[33][31] representing multiple different species with similar morphological traits.[5][3][4] The species granted the original epithet, costatum, was the species more narrowly described by Zingone et al. (2005) after reexamination of the type materials of S. costatum using electron microscopy and molecular analysis of rDNA.[3] Zingone et al., (2005) identified two distinct morphologies within the type material, describing the less abundant morphology as S. grevillei and the more abundant morphology as the original epithet, costatum.[3] The latter was assigned the original epithet due to its closer similarity to the specimen originally described by Greville, which he had conveniently marked.[3] The two morphologies differed in their frustule ultrastructures; including "the shape of FPPs [fultoportula processes], the type of interlocking between IFPPs [intercalary fultoportula processes] of sibling valves, and the cingular band ornamentation".[3] S. costatum sensu stricto (s. s.) can be used to describe the more narrowly defined S. costatum species to differentiate it from S. costatum sensu lato.[33] S. Costatum sensu stricto (s. s.) has also been referred to as S. costatum (Greville) Cleve emend. Zingone and Sarno.[34][30]

Distribution and habitat

Skeletonema costatum are found widely geographically distributed (apart from the Antarctic Ocean),[33] found around the world, including off the coasts of Hong Kong Island,[1] Florida, USA, Uruguay, Brazil,[5] Northern Queensland, Australia,[33] China, and the Sea of Japan.[34][26]

S. costatum primarily reside in the neritic zone and are commonly found in brackish waters as opposed to the more oceanic, S. tropicum.[23] S. costatum are frequently the dominant phytoplankton species responsible for red tide events.[6][35][36][37] Although the dominant species responsible for red tide events in a given area can change over time.[6][38] Locations of known red tide events where S. costatum were known to be dominant include the Yangtze River estuary.[39][7][40]

Yangtze River Estuary red tide outbreaks

S. costatum is one of the dominant species responsible for red tide outbreaks.[6] S. costatum blooms of these nature frequently occur in the Yangtze River estuary and adjacent waters in China.[7][6][40] Of the red tide outbreaks in the Yangtze River estuary between 1972 and 2009, S. costatum occurred during 20% of the 174 recorded outbreaks.[6] Over 50% of the outbreaks in this area occurred during May.[6] The frequency of red tide outbreaks in this area coincided with the concentration of dissolved inorganic nitrogen and PO4-P concentrations in this area, both increasing after 2002.[6] After 2000, outbreaks of areal extents larger than 1000 km2 became more common.[6] Nutrient applications from floods, fertilizers and other anthropogenic contributions in this area[41] is suspected to have contributed to the blooms[7].

Growth and environmental conditions

Temperature

S. costatum is most likely to grow in high temperature conditions. A temperature range of 2 [42] to 31.5 °C [43] was observed to support the growth of S. costatum, but members of this species grow optimally at 25 °C.[30] The strains of S. costatum from the Sea of Japan off the coast of Dokai Bay prefer warmer temperatures, only collected from water above 20 °C.[34] At this temperature, their specific growth rates were measured as above 1.0 d−1.[34]

Salinity

S. costatum can grow in salinity conditions of 0 to 35 psu.[30] As such, S. costatum can thrive in a variety of ocean environments ranging from oceanic to marine estuary and even riverine environments.[44][45] Its optimal growth was found to be at a salinity range of 18 to 35 psu.[44] The salinity tolerance of S. costatum is especially ideal in estuariane waters where salinities fluctuate, corroborated by the presence of this diatom as one of the dominant species in estuaries.[30]

Although some strains of S. costatum such as SZN B202 exhibit rapid growth rates in salinities of 1 to 2 psu, members of this species generally show decreased growth outside its optimal salinity range.[30] Decreased number of cells in a chain or decreased distance in between cells is observed at stress salinity conditions.[30]

Light levels

S. costatum is most likely to grow under conditions of high illumination. The highest growth rate was found to be 1.6 x 1016 quanta s−1cm−2, but there is still a positive growth rate in low-light conditions (0.02 x 1016 quanta s−1cm−2).[44] There is some debate over the different Skeletonema species and their classification, as many of these different species within the genus bloom in different seasons around the world.[46] Skeletonema costatum is a highly adaptable species and has the potential to bloom during all seasons and is more dependent on the water quality than photoperiod lengths for bloom formation, though it is especially common to have a large bloom during the early spring and late summer.[47][48][49][50]

High exposure to UVB radiation can have dramatic effects on the quality of S. costatum as a food source to marine invertebrates, marked by a decrease in fatty acid and amino acid contents of the individual S. costatum cells in these conditions.[51]

The high partial pressures of dissolved CO2 associated with climate change have a positive effect on the growth rate of S. costatum in the spring and fall, when there is equal parts light and dark in a day (12h light : 12 h dark).[52] The high partial pressure of CO2 was also found to reduce the growth rate of S. costatum in the winter (8h light : 16h dark) and had no effect on the growth rate of this marine diatom in the summer (16h light : 8h dark).[52]

At 20 °C, S. costatum can grow under irradiance of 7 to 406 μmol/m2s.[53] Photoinhibition is observed at 700 μmol/m2s, at which point a decrease in photosynthetic ability of the diatom is detected.[53]

Nutrients

S. costatum blooms in eutrophic waters that are often loaded with nitrogen, phosphorus, and other nutrients/minerals in both dissolved and particulate forms.[54] The eutrophic conditions that house S. costatum blooms are often limited in carbon dioxide, as there is heavy competition for this limiting resource.[8] It has been shown that nitrate enrichment and waters high in nitrate have the ability to stimulate S. costatum growth through the action of enhanced competitive photosynthetic activity in a CO2 limited environment.[55] Phosphate rich waters have also proven to have a stimulating effect on S. costatum growth rates in CO2-limited environments.[8] High concentrations of nitrates and phosphates also increase the amount of inorganic carbon in the form of bicarbonate fixed by S. costatum.[55][8]

Iron is an essential nutrient in primary production as it is used in processes of photosynthesis and is under high competition among marine diatoms. One of the reasons S. costatum is able to outcompete other primary producers is because of it's relatively high uptake rates of iron.[56] S. costatum also has a low cellular demand for iron, and thus is able to obtain this nutrient more efficiently than other phytoplankton.[56]  

Major viral pathogens

Skeletonema costatum-infecting virus (ScosV)

Skeletonema costatum-infecting virus (ScosV) is a novel algal virus isolated in 2008 from seawater samples taken in Jaran Bay, South Korea, which infects and lyses specific strains of S. costatum, particularly ME-SCM-1.[57] It was characterized in 2015 as having an icosahedral shape and a diameter of approximately 40 to 50 nm.[57][58] Upon infection of S. costatum, ScosV spends about less than 48 to 80 hours reproducing in the cytoplasm before causing lysis of host cells at a burst size range of 90 to 250 infectious units/cell.[57][58]

Ecological significance

Marine diatoms account for about 20% of the world's primary production [59] and considering that S. costatum is one of the most abundant species blooming in the ocean indicates that it is one of the major producers of oxygen.[60] S. costatum plays an important role in the acquisition of both organic and inorganic carbon (in the form of HCO3-) in our oceans,[8][9][10][11] collecting CO2 out of the atmosphere and reducing the effects of ocean acidification.

Eutrophic waters, as a result of aquaculture operations in nearshore marine environments such as shrimp farms,[61] create especially dominant conditions for S. costatum growth.[62][63] It has been reported that S. costatum dominated red tide algal blooms in these eutrophic waters associated with aquaculture have led to considerable depletion of phosphate that remained at a low level for a long time after the bloom disappeared.[54]

There is indication that S. costatum may be useful in the remediation of heavy metals from ocean ecosystems,[64] as it has a high affinity for iron and other heavy metals like manganese.[54]

Human applications

Aquaculture feed

Skeletonema costatum has has been cultivated for use in aquaculture, used as a feed for fish, shrimp, oysters, crab larvae and more.[16][17][18]

Production of biofuels

S. costatum is used in biofuel production because of its high lipid and fatty acid content[12][13][14][15][20], rapid growth rate[21][22], high photosynthetic efficiency[13][15], and high tolerance to variations in pH, temperature, and salinity levels[14][19]. When exposed to stress conditions such as depleted silicon and phosphate concentrations and high irradiation, it produces neutral lipids like triacylglycerol (TAG) which are best suitable for making biofuel.[12]

References

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