Vaucheria litorea

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Vaucheria litorea
Vaucheria sp sexial reproductive organ01.jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Clade: Diaphoretickes
Clade: SAR
Clade: Stramenopiles
Phylum: Gyrista
Subphylum: Ochrophytina
Class: Xanthophyceae
Order: Vaucheriales
Family: Vaucheriaceae
Genus: Vaucheria
Species:
V. litorea
Binomial name
Vaucheria litorea
Hofman ex. C.Agardh [1]

Vaucheria litorea is a species of yellow-green algae (Xanthophyceae). [2] It grows in a filamentous fashion (forming long tubular cells connected end to end). [2] V. litorea is a common intertidal species of coastal brackish waters and salt marshes of the Northern Atlantic, along the coasts of Europe, North America and New Zealand. [3] It is also found in the Eastern Pacific coasts of Washington state. It is found to be able to tolerate a large range of salinities, making it euryhaline. [4]

Contents

Taxonomy and nomenclature

The species belong to Vaucheria were initially documented within the genus Conferva, at that time consisting of 21 species, when reported by Linnaeus in 1753. Vaucheria litorea have been categorized under Vaucheriaceae. [5] Various historical classifications, found in older literature, situated Vaucheria among water molds and siphonous green algae. The species-level classification of Vaucheria has undergone considerable changes over the past century, involving the assignment of species to subgeneric sections and subsections. [5] [6] Presently, the genus Vaucheria is assigned to section Piloboloideae. [3] The recent taxonomy of the genus relies on a morphological species concept, wherein species are characterized based on morphology, particularly the shape, size, and arrangement of antheridia and oogonia. [7] Identifying closely related species poses challenges due to overlapping characteristics. [3] [7]

Description

V. litorea characterized by siphons with apical growth. The antheridia are cylindrical-acuminate, terminal on siphons, 400–650 μm long, and distributed in frequent sympodial clusters. The dark green, filamentous dioecious algae forms loose interwoven bundles or dense sods, attached to the substrate by branched rhizoids. Filaments are coenocytic, 70–95 μm thick, dichotomously branched, and lack transverse cell membranes. Reproduction is vegetative (fragmentation), asexual (large multinucleate synzoospores), and sexual (fertilization of a non-motile ovule by a motile multiflagellate antherozoid). [8]

Like most algae, V. litorea obtains its energy through photosynthesis taking place in chloroplasts. V. litorea belongs to the Stramenopiles, a group currently housing red algal secondary-derived plastids. [8] The chloroplasts of V. litorea are yellow-green, disc-shaped, small, and lack pyrenoids. [8] Also they contain the photosynthetic pigments Chlorophyll a, Chlorophyll c, β-Carotene, and the carotenoid diadinoxanthin. [9]

Plastid genome of V. litorea

The V. litorea plastid genome lacks the complete set of components for any of the four multi-subunit complexes of the photosynthetic electron transport chain (including photosystems I (PSI) and II (PSII), cytochrome b6/f complex, and ATP synthase) and the reductive pentose phosphate pathway (RPPP or Calvin–Benson cycle). [10] [11] Essential genes in the thylakoid-localized electron transport chain, such as those encoding the PSI and PSII light-harvesting complex pigment/proteins, the PSII Mn-stabilizing protein, and the redox-regulated γ-subunit of ATP synthase, are notably absent. The plastid-encoded enzyme for RPPP is limited to the carboxylating enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO). Unlike plants and green algae, both large and small subunits of RuBisCO are plastid-encoded in V. litorea. [8] [12]

Life history

The evolutionary history of Vaucheria indicates that the ancestral form produced antheridia and oogonia as separate structures, possibly adjacent. The presence of a gametophore bearing both an antheridium and an oogonium is considered a derived character state that evolved once in the ancestral Vaucheria. Additionally, the ancestral Vaucheria is inferred to have produced a single terminal pore on the antheridium, with multiple pores evolving independently on two occasions. The dioecious condition of Piloboloideae is suggested to be a derived state, and the presence of a gametophore distinguishes a monophyletic clade (sections Vaucheria, Corniculatae). [5]

Ecology

V. littorea is recognized as a photobiont (photosynthetic symbiont). Vaucheria litorea are consumed by the sea slug Elysia chlorotica , but are only partially digested by them in order to retain the photosynthetic chloroplasts in a process called kleptoplasty (plastid retention). The sea slug feeds on V. litorea and V. compacta , retaining the chloroplasts in storage in cells along the slug's digestive tract. [13] [14] The chloroplasts continue to photosynthesize, providing energy to the slug, and contribute to the unusual coloration of the sea slug by their distribution throughout the extensively branched gut. [14] The transmission of photosynthetic symbionts primarily occurs horizontally, with each generation of sea slug acquiring its photosynthetic partner anew from the surrounding environment. This association is not only specific but also obligate, as the sea slug cannot complete metamorphosis and mature into an adult without its algal prey and plastid uptake. The transmission to the germline represents a critical barrier for establishing a more permanent photosynthetic association in animals. [8] Specific recognition processes in the sea slug involve larvae requiring V. litorea filaments for settlement and metamorphosis, while adult development necessitates the uptake and retention of V. litorea plastids by cells in the digestive diverticula. [12]

Due to the secondary evolution of plastids, V. litorea's plastids are surrounded by four membranes. However, the outer two membranes are not readily observed in the sea slug. Only the plastids, referred to as kleptoplasts. [15] It was hypothesize that the evolution of kleptoplasty and photosynthesis in the sea slug parallels other tertiary-evolved photosynthetic organisms, involving endosymbiosis and potential horizontal gene transfer (HGT). [12] Kleptoplast activity in E. chlorotica remains evident even after months (up to ten months) of being starved of algal prey, indicating the presence of essential photosynthetic proteins. The decline in metabolic activity corresponds with aging, but photosystem I activity of kleptoplast thylakoids remains high for an extended period. [6] The long-term functioning of V. litorea plastids in E. chlorotica is intriguing, given the absence of algal nuclei in the sea slug. Plastid proteins, typically encoded by both the algal plastid and nuclear genomes, are crucial for photosynthesis, and the robustness of the plastids themselves likely contributes to their survival in the symbiosis. [16]

The plastid-encoded phosphoribulokinase (PRK) in V. litorea catalyzes the irreversible reaction generating the substrate ribulose-1,5-bisphosphate (RuBP) for Rubisco-dependent CO2 fixation supporting the Calvin cycle. To maintain the enzyme's activity, the PRK pre-protein must be de novo synthesized and imported from the cytosol. PRK is of interest due to its complex regulatory properties, with regulation characterized in only a few Stramenopiles, including diatoms and a raphidophyte. Dark inactivation of the Calvin cycle and PRK in V. litorea plastids is hypothesized to prevent futile cycling and support fatty acid biosynthesis and other carbon substrate synthesis. The long-term viability of the symbiotic association between V. litorea and E. chlorotica necessitates the acquisition of a prk gene that is thought to be through HGT. [15] However, it was shown that there are no signs of HGT between V. litorea and E. chlorotica. [16] The unique positions of three out of four introns in the V. litoreaprk gene, with the third intron at a homologous position as a conserved intron in green algae and haptophytes, provide additional evidence for the green algal origin of this gene in V. litorea and other chromalveolates. [15]

Related Research Articles

<span class="mw-page-title-main">Photosynthesis</span> Biological process to convert light into chemical energy

Photosynthesis is a biological process used by many cellular organisms to convert light energy into chemical energy, which is stored in organic compounds that can later be metabolized through cellular respiration to fuel the organism's activities. The term usually refers to oxygenic photosynthesis, where oxygen is produced as a byproduct and some of the chemical energy produced is stored in carbohydrate molecules such as sugars, starch, glycogen and cellulose, which are synthesized from endergonic reaction of carbon dioxide with water. Most plants, algae and cyanobacteria perform photosynthesis; such organisms are called photoautotrophs. Photosynthesis is largely responsible for producing and maintaining the oxygen content of the Earth's atmosphere, and supplies most of the biological energy necessary for complex life on Earth.

<span class="mw-page-title-main">Plastid</span> Plant cell organelles that perform photosynthesis and store starch

The plastid is a membrane-bound organelle found in the cells of plants, algae, and some other eukaryotic organisms. They are considered to be intracellular endosymbiotic cyanobacteria. Examples include chloroplasts, chromoplasts, and leucoplasts.

<span class="mw-page-title-main">Sacoglossa</span> Clade of gastropods

Sacoglossa, commonly known as the sacoglossans or the "solar-powered sea slugs", are a superorder of small sea slugs and sea snails, marine gastropod mollusks that belong to the clade Heterobranchia. Sacoglossans live by ingesting the cellular contents of algae, hence they are sometimes called "sap-sucking sea slugs".

<span class="mw-page-title-main">Kleptoplasty</span> Form of algae symbiosis

Kleptoplasty or kleptoplastidy is a process in symbiotic relationships whereby plastids, notably chloroplasts from algae, are sequestered by the host. The word is derived from Kleptes (κλέπτης) which is Greek for thief. The alga is eaten normally and partially digested, leaving the plastid intact. The plastids are maintained within the host, temporarily continuing photosynthesis and benefiting the host.

<span class="mw-page-title-main">Archaeplastida</span> Clade of eukaryotes containing land plants and some algae

The Archaeplastida are a major group of eukaryotes, comprising the photoautotrophic red algae (Rhodophyta), green algae, land plants, and the minor group glaucophytes. It also includes the non-photosynthetic lineage Rhodelphidia, a predatorial (eukaryotrophic) flagellate that is sister to the Rhodophyta, and probably the microscopic picozoans. The Archaeplastida have chloroplasts that are surrounded by two membranes, suggesting that they were acquired directly through a single endosymbiosis event by phagocytosis of a cyanobacterium. All other groups which have chloroplasts, besides the amoeboid genus Paulinella, have chloroplasts surrounded by three or four membranes, suggesting they were acquired secondarily from red or green algae. Unlike red and green algae, glaucophytes have never been involved in secondary endosymbiosis events.

<span class="mw-page-title-main">Photoinhibition</span>

Photoinhibition is light-induced reduction in the photosynthetic capacity of a plant, alga, or cyanobacterium. Photosystem II (PSII) is more sensitive to light than the rest of the photosynthetic machinery, and most researchers define the term as light-induced damage to PSII. In living organisms, photoinhibited PSII centres are continuously repaired via degradation and synthesis of the D1 protein of the photosynthetic reaction center of PSII. Photoinhibition is also used in a wider sense, as dynamic photoinhibition, to describe all reactions that decrease the efficiency of photosynthesis when plants are exposed to light.

<i>Elysia chlorotica</i> Species of gastropod

Elysia chlorotica is a small-to-medium-sized species of green sea slug, a marine opisthobranch gastropod mollusc. This sea slug superficially resembles a nudibranch, yet it does not belong to that clade. Instead it is a member of the clade Sacoglossa, the sap-sucking sea slugs. Some members of this group use chloroplasts from the algae they eat for photosynthesis, a phenomenon known as kleptoplasty. Elysia chlorotica is one species of such "solar-powered sea slugs". It lives in a subcellular endosymbiotic relationship with chloroplasts of the marine heterokont alga Vaucheria litorea.

<i>Elysia viridis</i> Species of gastropod

Elysia viridis, the sap-sucking slug, is a small-to-medium-sized species of green sea slug, a marine opisthobranch gastropod mollusc in the family Plakobranchidae.

<i>Elysia</i> (gastropod) Genus of gastropods

Elysia is a genus of sea slugs, marine gastropod molluscs in the family Plakobranchidae. These animals are colorful sea slugs, and they can superficially resemble nudibranchs, but are not very closely related to them. Instead they are sacoglossans, commonly known as sap-sucking slugs.

<i>Elysia crispata</i> Species of gastropod

Elysia crispata, common name the lettuce sea slug or lettuce slug, is a large and colorful species of sea slug, a marine gastropod mollusk.

<span class="mw-page-title-main">Photosynthetic reaction centre protein family</span>

Photosynthetic reaction centre proteins are main protein components of photosynthetic reaction centres (RCs) of bacteria and plants. They are transmembrane proteins embedded in the chloroplast thylakoid or bacterial cell membrane.

<i>Paulinella</i> Genus of single-celled organisms

Paulinella is a genus of at least eleven species including both freshwater and marine amoeboids. Like many members of euglyphids it is covered by rows of siliceous scales, and use filose pseudopods to crawl over the substrate of the benthic zone.

<span class="mw-page-title-main">Ochrophyte</span> Phylum of algae

Ochrophytes are the photosynthetic stramenopiles, a group of eukaryotes characterized by the presence of two unequal flagella, one of which has tripartite hairs called mastigonemes. In particular, ochrophytes are characterized by their plastids enclosed by four membranes, with thylakoids organized in piles of three, and the presence of chlorophylls a, c, and additional pigments such as β-carotene and xanthophylls. Ochrophytes are one of the most diverse lineages of eukaryotes, containing ecologically important algae such as brown algae and diatoms. They are classified either as phylum Ochrophyta or subphylum Ochrophytina within phylum Gyrista. Their plastid is of red algal origin.

<i>Elysia timida</i> Species of gastropod

Elysia timida is a species of sacoglossan sea slug, a marine opisthobranch gastropod mollusk. Found in the Mediterranean and nearby parts of the Atlantic, it is herbivorous, feeding on various algae in shallow water.

<i>Elysia pusilla</i> Species of gastropod

Elysia pusilla is a species of small sea slug, a marine gastropod mollusk in the family Plakobranchidae. It is a sacoglossan.

<i>Plakobranchus ocellatus</i> Species of gastropod

Plakobranchus ocellatus is a species of sea slug, a sacoglossan, a marine opisthobranch gastropod mollusk in the family Plakobranchidae. It is found in shallow water in the Indo-Pacific region.

The evolution of photosynthesis refers to the origin and subsequent evolution of photosynthesis, the process by which light energy is used to assemble sugars from carbon dioxide and a hydrogen and electron source such as water. The process of photosynthesis was discovered by Jan Ingenhousz, a Dutch-born British physician and scientist, first publishing about it in 1779.

<i>Costasiella ocellifera</i> Species of gastropod

Costasiella ocellifera is a small (5–13 mm) species of sea slug, a shell-less marine gastropod mollusk in the family Costasiellidae. Costasiella ocellifera, and other members of the Costasiellidae family are often mistakenly classified as nudibranchs because they superficially resemble other species of that group, but they are actually a part of the Sacoglossa superorder of sea slugs, also known as the “sap-sucking sea slugs,” "crawling leaves" or the "solar-powered sea slugs." C. ocellifera was discovered by Simroth in 1895, and was initially classified as Doto ocellifera. The Brazilian species, Costasiella liliana, is a synonym of C. ocellifera.Costasiella ocellifera shows long-term retention of functional kleptoplasty.

Rhodelphis is a single-celled archaeplastid that lives in aquatic environments and is the sister group to red algae and possibly Picozoa. While red algae have no flagellated stages and are generally photoautotrophic, Rhodelphis is a flagellated predator containing a non-photosynthetic plastid. This group is important to the understanding of plastid evolution because they provide insight into the morphology and biochemistry of early archaeplastids. Rhodelphis contains a remnant plastid that is not capable of photosynthesis, but may play a role in biochemical pathways in the cell like heme synthesis and iron-sulfur clustering. The plastid does not have a genome, but genes are targeted to it from the nucleus. Rhodelphis is ovoid with a tapered anterior end bearing two perpendicularly-oriented flagella.

<span class="mw-page-title-main">Photoautotrophism</span> Organisms that use light and inorganic carbon to produce organic materials

Photoautotrophs are organisms that use light energy and inorganic carbon to produce organic materials. Eukaryotic photoautotrophs absorb energy through the chlorophyll molecules in their chloroplasts while prokaryotic photoautotrophs use chlorophylls and bacteriochlorophylls present in free-floating thylakoids in their cytoplasm. All known photoautotrophs perform photosynthesis. Examples include plants, algae, and cyanobacteria.

References

  1. ↑ Searles, Richard B.; Schneider, Craig W. (1991). Seaweeds of the Southeastern United States: Cape Hatteras to Cape Canaveral. Durham, N.C: Duke University Press. ISBN   0-8223-1101-1.
  2. 1 2 Guiry, M.D.; Guiry, G.M. "Vaucheria litorea". AlgaeBase . World-wide electronic publication, National University of Ireland, Galway.
  3. 1 2 3 Muralidhar, Abishek; Broady, Paul A.; Macintyre, Duncan P.; Wilcox, Michael D.; Garrill, Ashley; Novis, Phil M. (2014). "Morphological and phylogenetic characterization of seven species of Vaucheria (Xanthophyceae), including two new species, from contrasting habitats in New Zealand". Phytotaxa. 186 (3): 117. doi:10.11646/phytotaxa.186.3.1. ISSN   1179-3163.
  4. ↑ Christensen, T. (1998). Salinity preference of twenty species of Vaucheria (Tribophyceae). Journal of the Marine Biological Association of the United Kingdom, 68, pp 531-545, doi:10.1017/S0025315400043381
  5. 1 2 3 Andersen, Robert A.; Bailey, J. Craig (2002). "PHYLOGENETIC ANALYSIS OF 32 STRAINS OF VAUCHERIA (XANTHOPHYCEAE) USING THE rbc L GENE AND ITS TWO FLANKING SPACER REGIONS 1". Journal of Phycology. 38 (3): 583–592. doi:10.1046/j.1529-8817.2002.01144.x. ISSN   0022-3646.
  6. 1 2 Rumpho, Mary E.; Summer, Elizabeth J.; Green, Brian J.; Fox, Theodore C.; Manhart, James R. (2001). "Mollusc/algal chloroplast symbiosis: how can isolated chloroplasts continue to function for months in the cytosol of a sea slug in the absence of an algal nucleus?". Zoology. 104 (3–4): 303–312. doi:10.1078/0944-2006-00036.
  7. 1 2 Entwisle, Tj (1988). "A monograph of Vaucheria (Vaucheriaceae, Chrysophyta) in south-eastern mainland Australia". Australian Systematic Botany. 1 (1): 1. doi:10.1071/SB9880001. ISSN   1030-1887.
  8. 1 2 3 4 5 Rumpho, Mary E.; Pelletreau, Karen N.; Moustafa, Ahmed; Bhattacharya, Debashish (2011). "The making of a photosynthetic animal". Journal of Experimental Biology. 214 (2): 303–311. doi:10.1242/jeb.046540. ISSN   1477-9145. PMC   3008634 . PMID   21177950.
  9. ↑ Stace, Clive A. (1980). Plant Taxonomy and Biosystematics . Cambridge University Press, 1991. ISBN   978-0-521-42785-2.
  10. ↑ Šantrůček, J. (2000). "Raghavendra, A.S. (Ed.): Photosynthesis. A Comprehensive Treatise". Photosynthetica. 38 (4): 530–530. doi:10.1023/A:1012434128938.
  11. ↑ Nelson, Nathan; Yocum, Charles F. (2006). "STRUCTURE AND FUNCTION OF PHOTOSYSTEMS I AND II". Annual Review of Plant Biology. 57 (1): 521–565. doi:10.1146/annurev.arplant.57.032905.105350. ISSN   1543-5008.
  12. 1 2 3 Rumpho, Mary E.; Worful, Jared M.; Lee, Jungho; Kannan, Krishna; Tyler, Mary S.; Bhattacharya, Debashish; Moustafa, Ahmed; Manhart, James R. (2008). "Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica". Proceedings of the National Academy of Sciences. 105 (46): 17867–17871. doi:10.1073/pnas.0804968105. ISSN   0027-8424. PMC   2584685 . PMID   19004808.
  13. ↑ Mujer, C.V., Andrews, D.L., Manhart, J.R., Pierce, S.K., & Rumpho, M.E. (1996). Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Cell Biology, 93, 12333-12338
  14. 1 2 Rumpho-Kennedy, M.E., Tyler, M., Dastoor, F.P., Worful, J., Kozlowski, R., & Tyler, M. (2006). Symbio: a look into the life of a solar-powered sea slug. Retrieved March 18, 2009, from http://sbe.umaine.edu/symbio/index.html Archived 2011-09-18 at the Wayback Machine
  15. 1 2 3 Rumpho, Mary E.; Pochareddy, Sirisha; Worful, Jared M.; Summer, Elizabeth J.; Bhattacharya, Debashish; Pelletreau, Karen N.; Tyler, Mary S.; Lee, Jungho; Manhart, James R.; Soule, Kara M. (2009). "Molecular Characterization of the Calvin Cycle Enzyme Phosphoribulokinase in the Stramenopile Alga Vaucheria litorea and the Plastid Hosting Mollusc Elysia chlorotica". Molecular Plant. 2 (6): 1384–1396. doi:10.1093/mp/ssp085. PMC   2782795 . PMID   19995736.
  16. 1 2 Bhattacharya, Debashish; Pelletreau, Karen N.; Price, Dana C.; Sarver, Kara E.; Rumpho, Mary E. (2013). "Genome Analysis of Elysia chlorotica Egg DNA Provides No Evidence for Horizontal Gene Transfer into the Germ Line of This Kleptoplastic Mollusc". Molecular Biology and Evolution. 30 (8): 1843–1852. doi:10.1093/molbev/mst084. ISSN   1537-1719. PMC   3708498 . PMID   23645554.
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