Karenia (dinoflagellate)

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Karenia
Karenia brevis.jpg
Karenia brevis
Scientific classification Red Pencil Icon.png
Clade: SAR
Infrakingdom: Alveolata
Phylum: Myzozoa
Superclass: Dinoflagellata
Class: Dinophyceae
Order: Gymnodiniales
Family: Kareniaceae
Genus: Karenia
Gert Hansen & Moestrup
Type species
Karenia brevis
(C.C.Davis) Gert Hansen & Moestrup

Karenia is a genus that consists of unicellular, photosynthetic, planktonic organisms found in marine environments. [1] The genus currently consists of 12 described species. [1] They are best known for their dense toxic algal blooms and red tides that cause considerable ecological and economical damage; some Karenia species cause severe animal mortality. [1] One species, Karenia brevis , is known to cause respiratory distress and neurotoxic shellfish poisoning (NSP) in humans. [1]

Contents

Taxonomy

The genus Karenia is named for Dr. Karen Steidinger for her exceptional contributions to dinoflagellate research. [1] She has spent many decades researching Karenia brevis. [1]

12 species have been described in the genus Karenia thus far: [1]

History of knowledge

Characteristic fish killings described by 15th and 16th century Spanish explorers were likely the earliest recorded sightings of Karenia. [2] Other major fish killings were documented in 1844 off of the coast of Florida. [1] Oda, in 1935, was the first to name any species in what is now the genus Karenia: [3] Gymnodinium mikimotoi but was later renamed Karenia mikimotoi. [1] Davis in 1948 was the first to document that the cause of the fish kills was the dinoflagellate Gymnodinium breve, [4] which was renamed Ptychodiscus brevis and since 2001 is now known as Karenia brevis. [1]

Description

Karenia are naked, flat, unicellular, photosynthetic cells that are quite pleomorphic: size tends to range from about 20–90 um. [1] The cell contains a straight apical groove, and differences in apical grooves (acrobases) are often used to distinguish between species. [5] Thecal plates are not present. [6] The cell body can be divided into an episome and a hyposome like other dinoflagellates. [6] Two dissimilar flagella that are involved in locomotion are present in the cingulum and sulcus. [6] The cytoplasm contains many yellow-green chloroplasts. [7] The plastid of Karenia is especially notable as it is the product of tertiary endosymbiosis, by uptake of a haptophyte. [7] Therefore, they lack the typical dinoflagellate pigment peridinin and have a plastid with pigments chlorophylls a+c and 19′-hexanoyloxyfucoxanthin, typically haptophyte pigments. [7] A nucleus is also found in the cell and its location and shape can distinguish between species. [5]

Habitat and ecology

Karenia is found throughout the world in both oceanic and coastal waters. [2] It is relatively sporadic in abundance, but it can form large blooms in the summer or fall which can have severe ecological and economical consequences. [8] These blooms are generally referred to as harmful algal blooms (HABs), but are also sometimes referred to as red tides. [2] Karenia is known to divide very slowly, but are able to form dense blooms probably due to their ability to swim quickly, which likely allows them access to higher concentrations of nutrients. [2] Many of these blooms consist of more than one type of Karenia species. [1] The cause of the blooms is still poorly understood. [8]

When a large bloom occurs, resources become limited, and this means greater competition for space and sunlight between several marine organisms—as the genus Karenia start dying they release their neurotoxins, which can kill fish and other organisms. [8] The dense blooms can also cause animal mortalities through anoxia. [8] Karenia brevis also causes distress in humans in the form of neurotoxic shellfish poisoning (NSP) which gets biomagnified up the food chain. [2] Karenia species produce a variety of toxins, with many probably producing more than one. [2]

Karenia are considered autotrophic organisms primarily, but some have been found to be mixotrophic as they can ingest microbes as well. [2]

Microbes have also been seen to be capable of attacking Karenia species, although their role in population dynamics is not well understood. [1]

Biology

Life cycle

Although the genus Karenia consists of 12 described species, most research on life cycles has been done on Karenia brevis which will be outlined here. Karenia follow the typical life cycle of a dinoflagellate with a motile, haploid, asexual cell with regular mitotic divisions. [1] This binary fission reproduction occurs once about every 2–10 days, and division occurs primarily at night (Brand et al., 2012). [1] They occasionally produce diploid planozygotes (mobile zygotes) implying they are capable of sexual reproduction. [1] They have been observed to be in what appears to be the process of conjugation, a type of unicellular sexual reproduction. [1] They can enter a hypnozygote cyst stage, which is an often thick walled, resting cyst that results from sexual fusion. [1] This occurs when environmental conditions are adverse and allows it to be dormant and spread to grow algal blooms elsewhere. [1]

Genetics

Karenia, like all organisms in the dinoflagellate group, are characteristic for their unique permanently condensed chromatin that lacks nucleosomes and histones. [9] The less tightly packed loops of DNA consist of actively transcribed DNA. [8] The haploid genome is large (about 30 times the size of humans), and usually contain a large quantity of repetitive, non-coding DNA. [9] They also portray a unique mitosis where the nuclear envelope stays intact and the mitotic spindle has extra nuclear microtubules that go through the nucleus through cytoplasmic channels. [9]

The genome of Karenia brevis is estimated to be about 1 x 10^11 bp, although the genome has not been sequenced in any members of this genus. [8]

Toxicity

Karenia are well known for their toxic blooms that kill fish, marine organisms, and other animals. These blooms, also called red tides, cause extensive ecological and economic damage. What causes these harmful algal blooms is still poorly understood. [1]

Karenia brevis is of particular importance to humans because it also can cause neurotoxic shellfish poisoning (NSP) and respiratory distress through accumulation of toxins in tissue. [1] These toxins are taken up by molluscs with no detrimental effects, but they distress the humans who ingest the molluscs. [1] The distress is caused by neurotoxins called brevetoxins. [10] Brevetoxins are lipid soluble and capable of biomagnification up the food chain. [10] They work by activating voltage-sensitive sodium channels and causing them to remain open for excessive amounts of time, which leads to uncontrolled depolarization of the neural membrane. [10] This results in persistent neuron firing. [10] No deaths have been recorded in association with brevetoxin, but severe effects have been noted, such as nausea, vomiting, and slurred speech. [10]

Related Research Articles

Red tide Common name for a worldwide phenomenon known as an algal bloom

Red tides are a phenomenon of discoloration of sea surface. It is a common name for harmful algal blooms occurring along coastal regions, which result from large concentrations of aquatic microorganisms, such as protozoans and unicellular algae . Terrestrial runoff, containing fertilizer, sewage and livestock wastes, transports abundant nutrients to the seawater and stimulates bloom events. Natural causes, such as river floods or upwelling of nutrients from the sea floor, often following massive storms, provide nutrients and trigger bloom events as well. Increasing coastal developments and aquaculture also contribute to the occurrence of red tides. Harmful algal blooms can occur worldwide, and natural cycles can vary regionally.

Algal bloom Rapid increase or accumulation in the population of planktonic algae

An algal bloom or algae bloom is a rapid increase or accumulation in the population of algae in freshwater or marine water systems. It is often recognized by the discoloration in the water from the algae's pigments. The term algae encompasses many types of aquatic photosynthetic organisms, both macroscopic multicellular organisms like seaweed and microscopic unicellular organisms like cyanobacteria. Algal bloom commonly refers to rapid growth of microscopic unicellular algae, not macroscopic algae. An example of a macroscopic algal bloom is a kelp forest.

Dinoflagellate unicellular algae with two flagella

The dinoflagellates are single-celled eukaryotes constituting the phylum Dinoflagellata and usually considered algae. Dinoflagellates are mostly marine plankton, but they also are common in freshwater habitats. Their populations vary with sea surface temperature, salinity, and depth. Many dinoflagellates are photosynthetic, but a large fraction of these are in fact mixotrophic, combining photosynthesis with ingestion of prey.

Paralytic shellfish poisoning Syndrome of shellfish poisoning

Paralytic shellfish poisoning (PSP) is one of the four recognized syndromes of shellfish poisoning, which share some common features and are primarily associated with bivalve mollusks. These shellfish are filter feeders and accumulate neurotoxins, chiefly saxitoxin, produced by microscopic algae, such as dinoflagellates, diatoms, and cyanobacteria. Dinoflagellates of the genus Alexandrium are the most numerous and widespread saxitoxin producers and are responsible for PSP blooms in subarctic, temperate, and tropical locations. The majority of toxic blooms have been caused by the morphospecies Alexandrium catenella, Alexandrium tamarense, Gonyaulax catenella and Alexandrium fundyense, which together comprise the A. tamarense species complex. In Asia, PSP is mostly associated with the occurrence of the species Pyrodinium bahamense.

Thin layers (oceanography)

Thin layers are concentrated aggregations of phytoplankton and zooplankton in coastal and offshore waters that are vertically compressed to thicknesses ranging from several centimeters up to a few meters and are horizontally extensive, sometimes for kilometers. Generally, thin layers have three basic criteria: 1) they must be horizontally and temporally persistent; 2) they must not exceed a critical threshold of vertical thickness; and 3) they must exceed a critical threshold of maximum concentration. The precise values for critical thresholds of thin layers has been debated for a long time due to the vast diversity of plankton, instrumentation, and environmental conditions. Thin layers have distinct biological, chemical, optical, and acoustical signatures which are difficult to measure with traditional sampling techniques such as nets and bottles. However, there has been a surge in studies of thin layers within the past two decades due to major advances in technology and instrumentation. Phytoplankton are often measured by optical instruments that can detect fluorescence such as LIDAR, and zooplankton are often measured by acoustic instruments that can detect acoustic backscattering such as ABS. These extraordinary concentrations of plankton have important implications for many aspects of marine ecology, as well as for ocean optics and acoustics. It is important to note that zooplankton thin layers are often found slightly under phytoplankton layers because many feed on them. Thin layers occur in a wide variety of ocean environments, including estuaries, coastal shelves, fjords, bays, and the open ocean, and they are often associated with some form of vertical structure in the water column, such as pycnoclines, and in zones of reduced flow.

<i>Karenia brevis</i> Species of dinoflagellate

Karenia brevis is a microscopic, single-celled, photosynthetic organism in the genus Karenia. It is a marine dinoflagellate commonly found in the waters of the Gulf of Mexico. It is the organism responsible for the "Florida red tides" that affect the Gulf coasts of Florida and Texas in the U.S., and nearby coasts of Mexico. K. brevis has been known to travel great lengths around the Florida peninsula and as far north as the Carolinas.

Brevetoxin Class of chemical compounds produced naturally

Brevetoxin (PbTx), or brevetoxins, are a suite of cyclic polyether compounds produced naturally by a species of dinoflagellate known as Karenia brevis. Brevetoxins are neurotoxins that bind to voltage-gated sodium channels in nerve cells, leading to disruption of normal neurological processes and causing the illness clinically described as neurotoxic shellfish poisoning (NSP).

Neurotoxic shellfish poisoning Syndrome of shellfish poisoning

Neurotoxic shellfish poisoning (NSP) is caused by the consumption of brevetoxins, which are marine toxins produced by the dinoflagellate Karenia brevis. These toxins can produce a series of gastrointestinal and neurological effects. Outbreaks of NSP commonly take place following harmful algal bloom (HAB) events, commonly referred to as "Florida red tide". Algal blooms are a naturally-occurring phenomenon, however their frequency has been increasing in recent decades at least in-part due to human activities, climate changes, and the eutrophication of marine waters. HABs have been occurring for all of documented history, evidenced by the Native Americans' understanding of the dangers of shellfish consumption during periods of marine bioluminescence. Blooms have been noted to occur as far north as North Carolina and are commonly seen alongside the widespread death of fish and sea birds. In addition to the effects on human health, the economic impact of HAB-associated shellfish toxin outbreaks can have significant economic implications as well due to not only the associated healthcare costs, but the adverse impact on the commercial shellfish industry.

Gymnodiniales Order of single-celled organisms

The Gymnodiniales are an order of dinoflagellates, of the class Dinophyceae. Members of the order are known as gymnodinioid or gymnodinoid. They are athecate, or lacking an armored exterior, and as a result are relatively difficult to study because specimens are easily damaged. Many species are part of the marine plankton and are of interest primarily due to being found in algal blooms. As a group the gymnodinioids have been described as "likely one of the least known groups of the open ocean phytoplankton."

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

Gonyaulax is a genus of dinoflagellates with the type species Gonyaulax spinifera Diesing. Gonyaulax belongs to red dinoflagellates and commonly causes red tides. It secretes a poisonous toxin known as "saxitoxin" which causes paralysis in humans.

<i>Akashiwo sanguinea</i> Species of single-celled organism

Akashiwo sanguinea is a species of marine dinoflagellates well known for forming blooms that result in red tides. The organism is unarmored (naked). Therefore, it lacks a thick cellulose wall, the theca, common in other genera of dinoflagellates. Reproduction of the phytoplankton species is primarily asexual.

Karenia mikimotoi is a dinoflagellate species from the genus Karenia. Its first appearance was in Japan in 1935 and since then, it has appeared in other parts of the world such as the east coast of the USA, Norway, and the English Channel.

Alexandrium catenella is a species of dinoflagellates. It is among the group of Alexandrium species that produce toxins that cause paralytic shellfish poisoning, and is a cause of red tide. These organisms have been found in the west coast of North America, Japan, Australia, and parts of South Africa.

Dinotoxins are a group of toxins which are produced by flagellate, aquatic, unicellular protists called dinoflagellates. Dinotoxin was coined by Hardy and Wallace in 2012 as a general term for the variety of toxins produced by dinoflagellates. Dinoflagellates are an enormous group of marine life, with much diversity. With great diversity comes many different toxins, however, there are a few toxins that multiple species have in common.

<i>Dinophysis acuminata</i> Species of dinoflagellate

Dinophysis acuminata is a marine plankton species of dinoflagellates that is found in coastal waters of the north Atlantic and Pacific oceans. The genus Dinophysis includes both phototrophic and heterotrophic species. D. acuminata is one of several phototrophic species of Dinophysis classed as toxic, as they produce okadaic acid which can cause diarrhetic shellfish poisoning (DSP). Okadiac acid is taken up by shellfish and has been found in the soft tissue of mussels and the liver of flounder species. When contaminated animals are consumed, they cause severe diarrhoea. D. acuminata blooms are constant threat to and indication of diarrhoeatic shellfish poisoning outbreaks.

Karenia papilionacea is a species from the genus Karenia, which are dinoflagellates. It was first discovered in New Zealand.

Karenia selliformis is a species from the genus Karenia, which are dinoflagellates. It was first discovered in New Zealand. Karenia selliformis produces the highly toxic gymnodimine, and as such is a potentially harmful ocean dweller. Gymnodimine is a nicotinic acetylcholine receptor-blocking phycotoxin, a source of shellfish poisoning.

Karenia bicuneiformis, also known as Karenia bidigitata is a microbial species from the genus Karenia, which are dinoflagellates. It was first discovered in New Zealand.

Mixotrophic dinoflagellate Plankton

Dinoflagellates are eukaryotic plankton, existing in marine and freshwater environments. Previously, dinoflagellates had been grouped into two categories, phagotrophs and phototrophs. Mixotrophs, however include a combination of phagotrophy and phototrophy. Mixotrophic dinoflagellates are a sub-type of planktonic dinoflagellates and are part of the phylum Dinoflagellata. They are flagellated eukaryotes that combine photoautotrophy when light is available, and heterotrophy via phagocytosis. Dinoflagellates are one of the most diverse and numerous species of phytoplankton, second to diatoms.

Jan H. Landsberg is a biologist, researcher, and author. Her professional research interests in biology have particular focus on aquatic animal and environmental health.

References

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  2. 1 2 3 4 5 6 7 Brand, Larry E.; Compton, Angela (2007). "Long-term increase in Karenia brevis abundance along the Southwest Florida Coast". Harmful Algae. 6 (2): 232–252. doi:10.1016/j.hal.2006.08.005. PMC   2330169 . PMID   18437245.
  3. Oda, M (1935). "The red tide of Gymnodinium mikimotoi n.sp. (MS.) and the effect of altering copper sulphate to prevent the growth of it". Dobutsugaku Zasshi, Zoological Society of Japan.
  4. Davis, CC (1948). "Gymnodinium brevis sp. nov., a cause of discolored water and animal mortalities in the Gulf of Mexico". Botanical Gazette. 109 (3): 358–360. doi:10.1086/335488. JSTOR   2472837. S2CID   84823699.
  5. 1 2 Yang, Z. B. (2000). "Karenia digitata sp. nov.(Gymnodiniales, Dinophyceae), a new harmful algal bloom species from the coastal waters of west Japan and Hong Kong". Phycologia. 39 (6): 463–470. doi:10.2216/i0031-8884-39-6-463.1. S2CID   85603177.
  6. 1 2 3 Haywood, Allison J.; Steidinger, Karen A.; Truby, Earnest W.; Bergquist, Patricia R.; Bergquist, Peter L.; Adamson, Janet; Mackenzie, Lincoln (2004-02-01). "Comparative morphology and molecular phylogenetic analysis of three new species of the genus Karenia (Dinophyceae) from New Zealand". Journal of Phycology. 40 (1): 165–179. doi:10.1111/j.0022-3646.2004.02-149.x. ISSN   1529-8817. S2CID   83753181.
  7. 1 2 3 Gabrielsen, T. M. (2011). "Genome Evolution of a Tertiary Dinoflagellate Plastid". PLOS ONE. 6 (4): e19132. Bibcode:2011PLoSO...619132G. doi: 10.1371/journal.pone.0019132 . PMC   3082547 . PMID   21541332.
  8. 1 2 3 4 5 6 Vargo, Gabriel A. (2009). "A brief summary of the physiology and ecology of Karenia brevis Davis (G. Hansen and Moestrup comb. nov.) red tides on the West Florida Shelf and of hypotheses posed for their initiation, growth, maintenance, and termination". Harmful Algae. 8 (4): 573–584. doi:10.1016/j.hal.2008.11.002.
  9. 1 2 3 "Why Sequence Karenia brevis".
  10. 1 2 3 4 5 Naar, Jerome; Bourdelais, Andrea; Tomas, Carmelo; Kubanek, Julia; Whitney, Philip L.; Flewelling, Leanne; Steidinger, Karen; Lancaster, Johnny; Baden, Daniel G. (2002). "A Competitive ELISA to Detect Brevetoxins from Karenia brevis (Formerly Gymnodinium breve) in Seawater, Shellfish, and Mammalian Body Fluid". Environmental Health Perspectives. 110 (2): 179–185. doi:10.1289/ehp.02110179. PMC   1240733 . PMID   11836147.

Further reading