Maullinia Ectocarpii
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''Maullinia'' is a
genus Genus (; : genera ) is a taxonomic rank above species and below family (taxonomy), family as used in the biological classification of extant taxon, living and fossil organisms as well as Virus classification#ICTV classification, viruses. In bino ...
of intracellular, phytomyxid
parasites Parasitism is a close relationship between species, where one organism, the parasite, lives (at least some of the time) on or inside another organism, the host, causing it some harm, and is adapted structurally to this way of life. The en ...
found across the Southern Hemisphere though primarily in Chile, The Prince Edward Islands, South Africa, Australia, and New Zealand. These parasites infiltrate the cells of their brown algal hosts via cytoplasmic extensions called plasmodia that divide synchronously, becoming increasingly multi-nucleate and engulfing the host cell
organelles In cell biology, an organelle is a specialized subunit, usually within a cell, that has a specific function. The name ''organelle'' comes from the idea that these structures are parts of cells, as organs are to the body, hence ''organelle,'' th ...
as they grow. Eventually, as the plasmodia fill the entire cell volume, the host cells become hypertrophied and grow to 3- 4x their original size, showing up as swollen appendages or galls on the host tissue at a macroscopic level. These swollen regions will burst alongside the mature ''Maullinia'' plasmodia, releasing biflagellated
zoospores A zoospore is a motile asexual spore that uses a flagellum for locomotion in aqueous or moist environments. Also called a swarm spore, these spores are created by some protists, bacteria, and fungi to propagate themselves. Certain zoospores are ...
to the inter- and extracellular space to disperse the infection further. Zoospores can come from sporangial plasmodia, as in ''M. ectocarpii'', or from resting spores, as in ''M. braseltonii''. As ''Maullinia'' can infect a wide range commercially important brown algal hosts, they present a significant threat to kelp farming and mariculture efforts. These infections could also cause significant harm on a global scale to natural populations, as they are able to disperse over long distances via
rafting Rafting and whitewater rafting are recreational outdoor activities which use an inflatable raft to navigate a river or other body of water. This is often done on whitewater or different degrees of rough water. Dealing with risk is often a ...
and tend to thrive in the cooler waters where kelp are often found.


Etymology

"''Maullinia''" refers to the
Maullín river Maullín River () is a river of Chile located in the Los Lagos Region. The river originates as the outflow of Llanquihue Lake, and flows generally southwestward, over a number of small waterfalls, emptying into the Gulf of Coronados.Image Science ...
near
Puerto Montt Puerto Montt (Mapuche: Meli Pulli) is a port city and commune in southern Chile, located at the northern end of the Reloncaví Sound in the Llanquihue Province, Los Lagos Region, 1,055 km to the south of the capital, Santiago. The commune ...
in Chile, from which the genus was first described. The
species epithet Specific name may refer to: * in Database management systems, a system-assigned name that is unique within a particular database In Taxonomy (biology), taxonomy, either of these two meanings, each with its own set of rules: * Specific name (botany) ...
for ''M.'' ''ectocarpii'' was chosen in reference to the host organism genus, ''
Ectocarpus ''Ectocarpus'' is a genus of filamentous brown alga that includes a model organism for the genomics of multicellularity. Among possible model organisms in the brown algae, ''Ectocarpus'' was selected for the relatively small size of its mature th ...
''''.'' In ''M. braseltonii'', the species epithet was chosen as a dedication to well-renowned phytomyxid specialist James P. Braselton.


Type species

''Maullinia ectocarpii'' I. Maier, E. R. Parodi, R. Westermeier et D. G. Müller sp. nov.


History of knowledge

For decades, brown algal kelps across the southern hemisphere have been described as having gall-forming infections of unknown origin. The cause of these galls was first investigated purely by chance, when a team of researchers from the
University of Konstanz The University of Konstanz () is a university in the city of Konstanz in Baden-Württemberg, Germany. Its main campus was opened on the Gießberg in 1972 after being founded in 1966. The university is Germany's southernmost university and is ...
, led by Dr. Ingo Maier, were conducting an
epiphytic An epiphyte is a plant or plant-like organism that grows on the surface of another plant and derives its moisture and nutrients from the air, rain, water (in marine environments) or from debris accumulating around it. The plants on which epiphyt ...
algal study in Chile. Some specimens of ''
Ectocarpus siliculosus ''Ectocarpus siliculosus'' is a filamentous brown alga. Its genome was the first brown macroalgal genome to be sequenced, with the expectation that ''E. siliculosus'' will serve as a genetic and genomic model for brown macroalgae. Ecology Th ...
'' in a Chilean mariculture plantation appeared to have parasitic infections, which piqued the research team's interest. After extensive field and laboratory culture experimentation, a new genus of phytomyxid was described as ''Maullinia''. This was the only phytomyxid parasite of brown algae known to science at the time, and was initially classified as a plasmodiophorid. Close to a decade later, while investigating gall-forming infections on fronds of the kelp ''Durvillaea'' ''antarctica'', researchers produced the first evidence of a second ''Maullinia'' species. Using
18S rRNA 18S ribosomal RNA (abbreviated 18S rRNA) is a part of the ribosomal RNA in eukaryotes. It is a component of the Eukaryotic small ribosomal subunit (40S) and the cytosolic homologue of both the 12S rRNA in mitochondria and the 16S rRNA in plas ...
molecular data from the parasites causing these gall-forming infections, they constructed a
phylogenetic tree A phylogenetic tree or phylogeny is a graphical representation which shows the evolutionary history between a set of species or taxa during a specific time.Felsenstein J. (2004). ''Inferring Phylogenies'' Sinauer Associates: Sunderland, MA. In ...
which placed the parasite as a sister species to ''M. ectocarpii''. However, not enough evidence was found to constitute a new species description at this time. A few years later, further molecular and morphological experimentation was carried out, providing enough evidence to classify this new ''Maullinia'' species as ''M. braseltonii''.


Ecology and habitat


Host interactions

The two species of ''Maullinia'' has been shown to successfully parasitize a wide range of brown algal hosts, spanning multiple brown algal orders, such as the
Ectocarpales Ectocarpales is a very large order (biology), order in the brown algae (class Phaeophyceae). The order includes families with pseudoparenchymatous (Splachnidiaceae) or true parenchymatous (Scytosiphonaceae) tissue. Pseudoparenchymatous refers t ...
,
Fucales The Fucales (fucoids) are an order in the brown algae (class Phaeophyceae). The list of families in the Fucales, as well as additional taxonomic information on algae, is publicly accessible at Algaebase. The class Phaeophyceae is included wit ...
, and
Laminariales Kelps are large brown algae or seaweeds that make up the order Laminariales. There are about 30 different genera. Despite its appearance and use of photosynthesis in chloroplasts, kelp is technically not a plant but a stramenopile (a group conta ...
''.'' A table of all known compatible hosts follows.


Impact on hosts

Markers of ''Maullinia'' infection vary across host species, but all exhibit
macroscopic The macroscopic scale is the length scale on which objects or phenomena are large enough to be visible with the naked eye, without magnifying optical instruments. It is the opposite of microscopic. Overview When applied to physical phenome ...
signs of hypertrophy. In
filamentous The word filament, which is descended from Latin ''filum'' meaning "Thread (yarn), thread", is used in English for a variety of thread-like structures, including: Astronomy * Galaxy filament, the largest known cosmic structures in the universe * ...
hosts (i.e., ''Ectocarpus''), or hosts in gametophytic stages with microthalli (i.e., ''Macrocystis''), swollen appendages can be found. These appendages are oblong to sub-spherical in shape, extending predominantly from the terminal cell on each main filament axis, but are also seen on the lateral branches. Appendages are unpigmented, with apical openings from which ''Maullinia'' zoospores are released. These appendages often occur in proximity to host
sporangia A sporangium (from Late Latin, ; : sporangia) is an enclosure in which spores are formed. It can be composed of a unicellular organism, single cell or can be multicellular organism, multicellular. Virtually all plants, fungus, fungi, and many ot ...
, increasing the host's sterility rate and number of abortive sporangia. In non-filamentous algae such as ''
Durvillaea ''Durvillaea'' is a genus of large brown algae in the monotypic family Durvillaeaceae. All members of the genus are found in the southern hemisphere, including Australia, New Zealand, South America, and various subantarctic islands. ''Durvillaea ...
'', infected during their mature
sporophyte A sporophyte () is one of the two alternation of generations, alternating multicellular organism, multicellular phases in the biological life cycle, life cycles of plants and algae. It is a diploid multicellular organism which produces asexual Spo ...
stages, large galls form on the fronds and stipe. These galls are irregular in shape, but most often are circular or ellipsoid with a diameter ranging from 0.5 cm to 7 cm. They are the result of cellular-level hypertrophy, which causes host cells to expand to be 3 – 4x their normal size. These hypertrophied cells are restricted to the sub-cortex, the region between the
cortex Cortex or cortical may refer to: Biology * Cortex (anatomy), the outermost layer of an organ ** Cerebral cortex, the outer layer of the vertebrate cerebrum, part of which is the ''forebrain'' *** Motor cortex, the regions of the cerebral cortex i ...
and the medullary tissue. Hypertrophied cells and the resulting macroscopic galls are paler than healthy tissue, with galls generally having a yellow-brown colouration. They may be solitary or clustered together, but clusters generally indicate a greater extent of ''Maullinia'' infection. Individuals which wash ashore tend to have ruptured in areas with these clustered galls, indicating that galls weaken the thallus and make it more susceptible to external damage. There is also strong evidence that ''Maullinia'', as a phytomyxid parasite, adversely affects the reproduction of its hosts. ''Maullinia'' infections of non-filamentous brown algae primarily target adult hosts, and are mostly absent during their reproductive periods. During non-reproductive periods, when adults dominate the populations, an infection rate of up to 40% can be seen. In other words, up to 9 individuals per square meter could be infected. These infections, regardless of whether the host is filamentous or non-filamentous, can increase
viral infection A viral disease (or viral infection) occurs when an organism's body is invaded by pathogenic viruses, and infectious virus particles (virions) attach to and enter susceptible cells. Examples include the common cold, gastroenteritis, COVID-19, t ...
rates as well. ''Maullinia'' infections do not appear to trigger significant defense mechanisms in their hosts, only passive protection from the presence of
fungal A fungus (: fungi , , , or ; or funguses) is any member of the group of eukaryotic organisms that includes microorganisms such as yeasts and molds, as well as the more familiar mushrooms. These organisms are classified as one of the tradit ...
endophytes An endophyte is an endosymbiont, often a bacterium or fungus, that lives within a plant for at least part of its life cycle without causing apparent disease. Endophytes are ubiquitous and have been found in all species of plants studied to date; ...
, and as such provide a vector for viral infections to enter the brown alga alongside ''Maullinia''.


Nutrition

As a parasitic genus, ''Maullinia'' derives its nutrition from the host cells it inhabits. Initially, the sole mode of nutrition was thought to be absorptive
osmotrophy Osmotrophy is a form of heterotrophic nutrition and a cellular feeding mechanism involving the direct absorption of dissolved organic compounds by osmosis. Organisms that use osmotrophy are called osmotrophs. Osmotrophy is used by diverse groups o ...
. In recent years however, new evidence has been revealed supporting intracellular
phagotrophy Phagocytosis () is the process by which a cell uses its plasma membrane to engulf a large particle (≥ 0.5 μm), giving rise to an internal compartment called the phagosome. It is one type of endocytosis. A cell that performs phagocytosis is ...
as the primary mode of nutrition, with osmotrophy as a secondary function. ''Maullinia'' appears to engulf the host organelles whole as it extends through the cell, with a preference for
plastids A plastid is a membrane-bound organelle found in the cells of plants, algae, and some other eukaryotic organisms. Plastids are considered to be intracellular endosymbiotic cyanobacteria. Examples of plastids include chloroplasts (used for photo ...
being clear. This preference could be due to several factors, namely active targeting by ''Maullinia,'' the widespread nature of plastids within brown algal cells, or simply a slower digestion process of these complex pigment-containing organelles. Evidence that there is some targeting of plastids comes from the host cell actively producing smaller plastids as the infection proceeds. Outside of the plastid preference, one of the first intracellular structures to be engulfed is the large storage
vacuole A vacuole () is a membrane-bound organelle which is present in Plant cell, plant and Fungus, fungal Cell (biology), cells and some protist, animal, and bacterial cells. Vacuoles are essentially enclosed compartments which are filled with water ...
. This vacuole contains many complex
polysaccharides Polysaccharides (), or polycarbohydrates, are the most abundant carbohydrates found in food. They are long-chain polymeric carbohydrates composed of monosaccharide units bound together by glycosidic linkages. This carbohydrate can react with wat ...
, and as such its consumption provides the infecting ''Maullinia'' with a boost in energy. This energy boost near the beginning of the infection, alongside the loss of a key energy source for the host cell, allows ''Maullinia'' to expand quickly.


Distribution and habitat

''Maullinia'' is found across much of the Southern Hemisphere, with infected brown algal populations in Chile, The Prince Edward Islands, South Africa, Australia, and New Zealand currently known. Within these regions ''Maullinia'' prevalence increases with
latitude In geography, latitude is a geographic coordinate system, geographic coordinate that specifies the north-south position of a point on the surface of the Earth or another celestial body. Latitude is given as an angle that ranges from −90° at t ...
, becoming more dominant in southern populations as compared to more tropical ones. This is likely due to a combination of two key factors: the increased density of southern populations and increased ''Maullinia''
virulence Virulence is a pathogen's or microorganism's ability to cause damage to a host. In most cases, especially in animal systems, virulence refers to the degree of damage caused by a microbe to its host. The pathogenicity of an organism—its abili ...
in cooler waters. While many parasites prefer warmer environments, ''Maullinia'' appears to thrive in lower temperatures, having greatest infection rates during the winter months and at greater latitude. The two species of ''Maullinia'' appear to have some preference for habitat, based on the brown algal hosts which they each primarily infect. ''M. ectocarpii'' prefers sandy, shallow, sheltered regions where more filamentous brown algae tend to thrive. However, ''M. ectocarpii'' is a more generalist species and can adapt to more rocky intertidal species such as '' Durvillaea amatheiae'' and '' Durvillaea potatorum''. ''M. braseltonii'' is much more specialist, and exclusively infects ''Durvillaea'' hosts stemming from rocky intertidal habitats. As many ''Durvillaea'' species are buoyant, ''M. braseltonii'' is often found infecting drift as well. The role of drift in distributing ''Maullinia'' and providing a vector for novel infections is critical. Rafting is the primary way by which new populations of brown algae are infected by ''Maullinia'', and this process is supported by the
physiological Physiology (; ) is the science, scientific study of function (biology), functions and mechanism (biology), mechanisms in a life, living system. As a branches of science, subdiscipline of biology, physiology focuses on how organisms, organ syst ...
changes infected hosts undergo. With the hypertrophied cells forming galls, a greater buoyancy is achieved in infected individuals, allowing them a wider distribution capability. The likelihood of the mechanism is strengthened by the genetic evidence which links the New Zealand population of ''Maullinia'' to the Chile population. The role of rafting, alongside the widespread populations separated by thousands of kilometers, implies that ''Maullinia'' may be capable of achieving global distribution along cold-temperate coasts.


Description


Life cycle

Life cycles in ''Maullinia'' are not completely understood, nor has sexual reproduction been observed. ''M. ectocarpii'' and ''M. braseltonii'' seem to produce two different forms of plasmodia which develop into unique structures and zoospores not yet observed in the other. Outside of these two plasmodial forms, the life cycle is largely identical.  


Cysts

Encystment occurs when a ''Maullinia'' biflagellated stage settles on a compatible host, and can begin the infection process. Cysts are ellipsoid to kidney-shaped, being approximately 5.8 ± 0.7 μm long and 2.5 ± 0.2 μm wide. They have
chitinous Chitin ( C8 H13 O5 N)n ( ) is a long-chain polymer of ''N''-acetylglucosamine, an amide derivative of glucose. Chitin is the second most abundant polysaccharide in nature (behind only cellulose); an estimated 1 billion tons of chitin are pr ...
cell walls which break open at one end to allow the adhesorium, an infection apparatus, to extend. The adhesorium has no cell wall and develops from a beak-like shape into a narrow neck of 5 – 7 μm in length which punctures the host cell wall. From here, the cyst contents are injected into the host cell cytoplasm, and plasmodial formation begins.


Plasmodia

Once cyst contents have been injected into the host cytoplasm, synchronous nuclear divisions occur rapidly to produce large multinucleate plasmodia within the host cell. Each plasmodial nucleus is spherical and contains a distinct, centric nucleolus. Plasmodia continue to grow, via cruciform and non-cruciform mitotic divisions, engulfing host organelles and causing strong host cell hypertrophy. The host nucleus becomes engorged as a result of the hypertrophy, and eventually ceases division. This growth may alter the hosts metabolic functioning, collecting energy-rich compounds within the cell to help feed the ''Maullinia'' parasite, although this theory is not proven. After enough plasmodial growth occurs and the host cell is entirely filled, a lobose structure is adopted and plasmodial differentiation occurs.


Sporangia & sporangial zoospores (seen in ''M. ectocarpii'')

Mature plasmodia transform into a single sporangium, which develops near the host cell wall and becomes attached to it via deposition of a fine, but dense, fibrillar wall-like material. The size and shape of these sporangia are variable both within and across host species, but on average are club-shaped, 40 – 93 μm long and 27–46 μm wide. In ''Ectocarpus'', these sporangia occur in clusters that mirror the hosts' own growth pattern. Each sporangium produces several hundred zoospores. Sporangia produce sporangial zoospores, pyriform cells 4.6 ± 0.7 μm long length, 2.3 ± 0.4 μm wide with thick walls and 2
flagella A flagellum (; : flagella) (Latin for 'whip' or 'scourge') is a hair-like appendage that protrudes from certain plant and animal sperm cells, from fungal spores ( zoospores), and from a wide range of microorganisms to provide motility. Many pr ...
extending from the broad part of the cell. These flagella are of unequal length, with the longer flagellum being more posteriorly oriented and undulating, while the shorter one is more anteriorly oriented and oblique to the midline. Both flagella have short hair tips along them. Sporangial zoospore nuclei have an abundance of condensed chromatin, but no nucleoli. These zoospores are extremely motile and exit singly from a single apical opening on the sporangium. Once released, they disperse and make contact with hosts to begin encystment again.


Resting spores (seen in ''M. braseltonii'')

Resting spores A resting spore is a resistant cell, adapted to survive adverse environmental conditions. Resting spore is a term commonly applied to both diatoms and fungi. In fungi and oomycetes A resting spore can be a spore created by fungi which is thickly ...
allow for survival in antagonistic environments, which allows ''M. braseltonii'' to be more specific about which hosts it chooses to infect as a host cell is not needed for resting spore survival. The plasmodium begins resting spore development by concentrating cytoplasm around the nucleus, allowing the thick, 3-layered wall to start forming. Initially, these resting spores are very irregular and globose to elliptic, but become more regularly spherical as they mature. They have no colour, and will wait to release zoospores until conditions are optimal. These zoospores may be differently structured than their sporangial counterparts, but they have yet to be observed.


Practical importance

''Maullinia'' has hosts of high commercial importance, such as ''
Macrocystis ''Macrocystis'' is a monospecific genus of kelp (large brown algae) with all species now synonymous with ''Macrocystis pyrifera''. It is commonly known as giant kelp or bladder kelp. This genus contains the largest of all the Phaeophyceae or b ...
'', and as such have the potential of causing devastating effects if an infection were able to spread into a gametophyte mariculture supporting a ''Macrocystis'' kelp farm. Examples have been seen already, with the initial description of ''Maullinia'' occurring on an infected Chilean ''Ectocarpus'' mariculture. These kinds of infections could compound with the delivery of brown algal viruses alongside the parasite, decimating entire kelp cultures in the process. In addition to its known effects on brown algal hosts, ''Maullinia'' has the ability to infect a wide range of hosts that could possibly bridge the marine-terrestrial gap. Phytomyxid parasites have been proven capable of shifting hosts across
kingdoms Kingdom commonly refers to: * A monarchic state or realm ruled by a king or queen. ** A monarchic chiefdom, represented or governed by a king or queen. * Kingdom (biology), a category in biological taxonomy Kingdom may also refer to: Arts and me ...
(i.e., from brown algae to angiosperms), and could this introduce completely novel parasites to terrestrial environments.


Species

* ''Maullinia ectocarpii'' I. Maier, E. R. Parodi, R. Westermeier et D. G. Müller 2000 * ''Maullinia braseltonii'' P. Murúa, F. Goecke et S. Neuhauser 2017


References

* * {{Taxonbar, from=Q25366523 Endomyxa Rhizaria genera