A trophosome is a highly vascularised organ found in some animals that houses symbiotic

bacteria Bacteria (; : bacterium) are ubiquitous, mostly free-living organisms often consisting of one Cell (biology), biological cell. They constitute a large domain (biology), domain of Prokaryote, prokaryotic microorganisms. Typically a few micr ...

that provide food for their host. Trophosomes are contained by the

coelom The coelom (or celom) is the main body cavity in many animals and is positioned inside the body to surround and contain the digestive tract and other organs. In some animals, it is lined with mesothelium. In other animals, such as molluscs, i ...

of tube worms (family

Siboglinidae Siboglinidae is a family (biology), family of polychaete Annelida, annelid worms whose members made up the former phylum, phyla Pogonophora and Vestimentifera (the giant tube worms). The family is composed of around 100 species of vermiform creatu ...

, e.g. the

giant tube worm ''Riftia pachyptila'', commonly known as the giant tube worm and less commonly known as the giant beardworm, is a marine invertebrate in the phylum Annelida (formerly grouped in phylum Pogonophora and Vestimentifera) related to tube worms ...

Riftia pachyptila ''Riftia pachyptila'', commonly known as the giant tube worm and less commonly known as the giant beardworm, is a marine invertebrate in the phylum Annelida (formerly grouped in phylum Pogonophora and Vestimentifera) related to tube worms ...

'') and in the body of symbiotic

flatworm Platyhelminthes (from the Greek language, Greek πλατύ, ''platy'', meaning "flat" and ἕλμινς (root: ἑλμινθ-), ''helminth-'', meaning "worm") is a Phylum (biology), phylum of relatively simple bilaterian, Segmentation (biology), ...

s of the genus '' Paracatenula''.

Organization

Initially, the trophosome in frenulates and

vestimentiferan Siboglinidae is a family of polychaete annelid worms whose members made up the former phyla Pogonophora and Vestimentifera (the giant tube worms). The family is composed of around 100 species of vermiform creatures which live in thin tubes buried ...

s, which are now classified as members of the

, had been identified as a

mesoderm The mesoderm is the middle layer of the three germ layers that develops during gastrulation in the very early development of the embryo of most animals. The outer layer is the ectoderm, and the inner layer is the endoderm.Langman's Medical ...

al tissue. The discovery of

inside the trophosomal tissue only occurred in 1981 when the ultrastructure of trophosome of several frenulate species and of '' Sclerolinum brattstromi'' was studied. The

bacteriocyte A bacteriocyte ( Greek for ''bacteria cell''), also known as a mycetocyte, is a specialized adipocyte found primarily in certain insects such as aphids, tsetse flies, German cockroaches, weevils, and ants. These cells contain endosymbioti ...

s and symbionts composed of 70.5% and 24.1% of the trophosome's

volume Volume is a measure of regions in three-dimensional space. It is often quantified numerically using SI derived units (such as the cubic metre and litre) or by various imperial or US customary units (such as the gallon, quart, cubic inch) ...

respectively. Generally, trophosome extends over the entire trunk region between the two longitudinal blood vessels from immediately posterior to the ventral ciliary band of the forepart to the posterior end of the trunk delineated by the septum between trunk and first

opisthosoma The opisthosoma is the posterior part of the body in some arthropods, behind the prosoma ( cephalothorax). It is a distinctive feature of the subphylum Chelicerata (arachnids, horseshoe crabs and others). Although it is similar in most respects ...

l segment. The trophosome can be differentiated between anterior and a posterior area due to incremental changes in

host A host is a person responsible for guests at an event or for providing hospitality during it. Host may also refer to: Places * Host, Pennsylvania, a village in Berks County * Host Island, in the Wilhelm Archipelago, Antarctica People * ...

tissue organization, the amount of

s, the size and shape of symbionts. The trophosome consisted anteriorly of a small number of

s and extensive mesenchyma, while the posterior of trophosome subsequently consisted of a large population of

s and a peripheral

peritoneum The peritoneum is the serous membrane forming the lining of the abdominal cavity or coelom in amniotes and some invertebrates, such as annelids. It covers most of the intra-abdominal (or coelomic) organs, and is composed of a layer of mesotheli ...

Bacteriocytes and symbionts

The

cytoplasm The cytoplasm describes all the material within a eukaryotic or prokaryotic cell, enclosed by the cell membrane, including the organelles and excluding the nucleus in eukaryotic cells. The material inside the nucleus of a eukaryotic cell a ...

is abundant in

glycogen Glycogen is a multibranched polysaccharide of glucose that serves as a form of energy storage in animals, fungi, and bacteria. It is the main storage form of glucose in the human body. Glycogen functions as one of three regularly used forms ...

and contains some electron-dense, round-shape granules.

Mitochondria A mitochondrion () is an organelle found in the cells of most eukaryotes, such as animals, plants and fungi. Mitochondria have a double membrane structure and use aerobic respiration to generate adenosine triphosphate (ATP), which is us ...

and the rough endoplastic reticulum are low in number. Throughout the anterior trophosome region, the nuclei were mainly oval but irregularity in the shape of the nuclei is observed in the posterior trophosome region. The

cell wall A cell wall is a structural layer that surrounds some Cell type, cell types, found immediately outside the cell membrane. It can be tough, flexible, and sometimes rigid. Primarily, it provides the cell with structural support, shape, protection, ...

of the symbionts composed of an outer membrane and a

cytoplasmic membrane The cell membrane (also known as the plasma membrane or cytoplasmic membrane, and historically referred to as the plasmalemma) is a biological membrane that separates and protects the cytoplasm, interior of a Cell (biology), cell from the extrac ...

typical of

gram-negative bacteria Gram-negative bacteria are bacteria that, unlike gram-positive bacteria, do not retain the Crystal violet, crystal violet stain used in the Gram staining method of bacterial differentiation. Their defining characteristic is that their cell envelo ...

. Symbionts were often embedded separately in the symbiosome membrane adjacent to the

bacterial cell wall A cell wall is a structural layer that surrounds some cell types, found immediately outside the cell membrane. It can be tough, flexible, and sometimes rigid. Primarily, it provides the cell with structural support, shape, protection, and functi ...

except when they are proliferating. In such case, proliferating symbionts are frequently found in the anterior trophosome region.

Structural organization

The Ultrastructure of the Trophosome Region

In frenulates

In frenulates, the trophosome is limited to the post-annular portion of the trunk. While a structural variant of the frenulate trophosome seems to occur, this organ typically consists of two

epithelium Epithelium or epithelial tissue is a thin, continuous, protective layer of cells with little extracellular matrix. An example is the epidermis, the outermost layer of the skin. Epithelial ( mesothelial) tissues line the outer surfaces of man ...

and blood spaces sandwiched between the basal matrix of the

epithelia Epithelium or epithelial tissue is a thin, continuous, protective layer of cells with little extracellular matrix. An example is the epidermis, the outermost layer of the skin. Epithelial ( mesothelial) tissues line the outer surfaces of many ...

in which the inner one is composed of

s and the outer one is the

coelomic A body cavity is any space or compartment, or potential space, in an animal body. Cavities accommodate organs and other structures; cavities as potential spaces contain fluid. The two largest human body cavities are the ventral body cavity, a ...

lining. The trophosome of ''Sclerolinum brattstromi'' consists of a centre of

s surrounded by blood space and

In vestimentiferans

The trophosome of

s is a complex, multi-lobed body with a vascular blood system that covers the entire trunk region. Each lobule consists of a tissue of

s enclosed by an aposymbiotic coelothel. It is traversed by an axial efferent blood vessel, and is supplied with ramifying peripheral afferent blood vessels.

In ''Osedax''

In ''

Osedax ''Osedax'' is a genus of deep-sea siboglinid polychaetes, commonly called boneworms, zombie worms, or bone-eating worms. ''Osedax'' is Latin for "bone-eater". The name alludes to how the worms bore into the bones of whale carcasses to reach en ...

'', only the female has the trophosome. The trophosome in ''Osedax'' is made up of non symbiotic bacteria that reside between the muscle layer of the body's wall and the

in the ovisac and root regions; therefore, it is derived from the somatic mesoderm.

Trophosome color

The host lacks entirely a

digestive system The human digestive system consists of the gastrointestinal tract plus the accessory organs of digestion (the tongue, salivary glands, pancreas, liver, and gallbladder). Digestion involves the breakdown of food into smaller and smaller compone ...

but derives all the essential

nutrient A nutrient is a substance used by an organism to survive, grow and reproduce. The requirement for dietary nutrient intake applies to animals, plants, fungi and protists. Nutrients can be incorporated into cells for metabolic purposes or excret ...

s from its

endosymbiont An endosymbiont or endobiont is an organism that lives within the body or cells of another organism. Typically the two organisms are in a mutualism (biology), mutualistic relationship. Examples are nitrogen-fixing bacteria (called rhizobia), whi ...

. The host in turn provides the

with all necessary

inorganic compound An inorganic compound is typically a chemical compound that lacks carbon–hydrogen bonds⁠that is, a compound that is not an organic compound. The study of inorganic compounds is a subfield of chemistry known as ''inorganic chemistry''. Inorgan ...

s for chemolithoautotrophy. Inorganic elements, such as

hydrogen sulphide Hydrogen sulfide is a chemical compound with the formula . It is a colorless chalcogen-hydride gas, and is toxic, corrosive, and flammable. Trace amounts in ambient atmosphere have a characteristic foul odor of rotten eggs. Swedish chemist Ca ...

, are

oxidized Redox ( , , reduction–oxidation or oxidation–reduction) is a type of chemical reaction in which the oxidation states of the reactants change. Oxidation is the loss of electrons or an increase in the oxidation state, while reduction is ...

to produce energy for

carbon fixation Biological carbon fixation, or сarbon assimilation, is the Biological process, process by which living organisms convert Total inorganic carbon, inorganic carbon (particularly carbon dioxide, ) to Organic compound, organic compounds. These o ...

. Trophosome tissue containing large quantities of concentrated

sulphur Sulfur (American spelling and the preferred IUPAC name) or sulphur (English in the Commonwealth of Nations, Commonwealth spelling) is a chemical element; it has Symbol (chemistry), symbol S and atomic number 16. It is abundance of the chemical ...

has a light yellowish color. During sulfur limitation, i.e. when energy supply is reduced due to low concentrations of environmental sulfur, the stored sulfur is absorbed and the trophosome appears much darker. Therefore, the energetic state of the symbiosis can be specifically interpreted from the color of the trophosome.

Trophosome growth

Trophosome tissue development happens by

stem cell In multicellular organisms, stem cells are undifferentiated or partially differentiated cells that can change into various types of cells and proliferate indefinitely to produce more of the same stem cell. They are the earliest type of cell ...

s in the center of each lobule, contributing to new lobules as well as the regeneration of

s circulating from the center to the periphery of each lobule through which

apoptosis Apoptosis (from ) is a form of programmed cell death that occurs in multicellular organisms and in some eukaryotic, single-celled microorganisms such as yeast. Biochemistry, Biochemical events lead to characteristic cell changes (Morphology (biol ...

happens. The trophosome tissue thus not only shows high levels of proliferation but also fairly small levels of apoptosis. Furthermore, symbionts in the periphery are constantly digested and replaced by separating symbionts in the middle.

Lysophosphatidylethanolamine A lysophosphatidylethanolamine (LPE) is a chemical compound derived from a phosphatidylethanolamine, which is typical of cell membranes. LPE results from partial hydrolysis of phosphatidylethanolamine, which removes one of the fatty acid groups. Th ...

s and

free fatty acids In chemistry, in particular in biochemistry, a fatty acid is a carboxylic acid with an aliphatic chain, which is either saturated or unsaturated. Most naturally occurring fatty acids have an unbranched chain of an even number of carbon atoms, f ...

are the products of

phospholipid Phospholipids are a class of lipids whose molecule has a hydrophilic "head" containing a phosphate group and two hydrophobic "tails" derived from fatty acids, joined by an alcohol residue (usually a glycerol molecule). Marine phospholipids typ ...

hydrolysis Hydrolysis (; ) is any chemical reaction in which a molecule of water breaks one or more chemical bonds. The term is used broadly for substitution reaction, substitution, elimination reaction, elimination, and solvation reactions in which water ...

phospholipase A phospholipase is an enzyme that hydrolyzes phospholipids into fatty acids and other lipophilic substances. There are four major classes, termed A, B, C, and D, which are distinguished by the type of reaction which they catalyze: *Phospholipase ...

s through the normal degradation of the membranes. The presence of fairly high levels of

lysophosphatidylethanolamine A lysophosphatidylethanolamine (LPE) is a chemical compound derived from a phosphatidylethanolamine, which is typical of cell membranes. LPE results from partial hydrolysis of phosphatidylethanolamine, which removes one of the fatty acid groups. Th ...

s and

fatty acid In chemistry, in particular in biochemistry, a fatty acid is a carboxylic acid with an aliphatic chain, which is either saturated and unsaturated compounds#Organic chemistry, saturated or unsaturated. Most naturally occurring fatty acids have an ...

s in trophosome indicate the high turnover of host and symbiont cells in the trophosome contributing to tissue and membrane degradation.

Chemolithoautotrophy

In both these animals, the symbiotic bacteria that live in the trophosome oxidize

sulfur Sulfur ( American spelling and the preferred IUPAC name) or sulphur ( Commonwealth spelling) is a chemical element; it has symbol S and atomic number 16. It is abundant, multivalent and nonmetallic. Under normal conditions, sulfur atoms ...

sulfide Sulfide (also sulphide in British English) is an inorganic anion of sulfur with the chemical formula S2− or a compound containing one or more S2− ions. Solutions of sulfide salts are corrosive. ''Sulfide'' also refers to large families o ...

found in the worm's environment and produce organic molecules by carbon dioxide fixation that the hosts can use for nutrition and as an energy source. This process is known as

chemosynthesis In biochemistry, chemosynthesis is the biological conversion of one or more carbon-containing molecules (usually carbon dioxide or methane) and nutrients into organic matter using the oxidation of inorganic compounds (e.g., hydrogen gas, hydrog ...

or chemolithoautotrophy.

Carbon transfer

Two different modes of carbon transfer from the symbionts to the host have been suggested. * The transfer of nutrients through

digestion Digestion is the breakdown of large insoluble food compounds into small water-soluble components so that they can be absorbed into the blood plasma. In certain organisms, these smaller substances are absorbed through the small intestine into th ...

of bacteria. This model is supported by the ultrastructural studies of the trophosome showing symbionts in various stages of

lysis Lysis ( ; from Greek 'loosening') is the breaking down of the membrane of a cell, often by viral, enzymic, or osmotic (that is, "lytic" ) mechanisms that compromise its integrity. A fluid containing the contents of lysed cells is called a ...

. * The transfer of nutrients through small nutritive molecules released by

. The only strong evidence for this hypothesis is the discovery by Felbeck and Jarchow (1998) that the distilled symbionts release substantial quantities of

succinate Succinic acid () is a dicarboxylic acid with the chemical formula (CH2)2(CO2H)2. In living organisms, succinic acid takes the form of an anion, succinate, which has multiple biological roles as a metabolic intermediate being converted into Fuma ...

and, to a lesser degree,

glutamate Glutamic acid (symbol Glu or E; known as glutamate in its anionic form) is an α-amino acid that is used by almost all living beings in the biosynthesis of proteins. It is a Essential amino acid, non-essential nutrient for humans, meaning that ...

in vitro, indicating that these could be the main compounds transmitted from the symbionts to the host

in vivo Studies that are ''in vivo'' (Latin for "within the living"; often not italicized in English) are those in which the effects of various biological entities are tested on whole, living organisms or cells, usually animals, including humans, an ...

Carbon fixation

Trophosome observed high activity of ribulose-1,5-bisphosphate carboxylase / oxygenase and ribulose 5-phosphate kinase, the enzymes of the Calvin-Benson fixation cycle. It is important to notice that the observed activities of two enzymes, ribulose-1,5-bisphosphate carboxylase / oxygenase and ribulose 5-phosphate kinase, are present at high concentrations in the trophosome, but are absent in the

muscle Muscle is a soft tissue, one of the four basic types of animal tissue. There are three types of muscle tissue in vertebrates: skeletal muscle, cardiac muscle, and smooth muscle. Muscle tissue gives skeletal muscles the ability to muscle contra ...

. Furthermore,

rhodanese Rhodanese is a mitochondrial enzyme that detoxifies cyanide (CN−) by converting it to thiocyanate (SCN−, also known as "rhodanate"). In enzymatology, the common name is listed as thiosulfate sulfurtransferase (). The diagram on the right s ...

, APSreductase, and ATP-sulfurylase are involved in

adenosine triphosphate Adenosine triphosphate (ATP) is a nucleoside triphosphate that provides energy to drive and support many processes in living cell (biology), cells, such as muscle contraction, nerve impulse propagation, and chemical synthesis. Found in all known ...

synthesis using the energy found in

compounds such as

. These findings contribute to the conclusion that the

symbiont Symbiosis (Ancient Greek : living with, companionship < : together; and ''bíōsis'': living) is any type of a close and long-term biological interaction, between two organisms of different species. The two organisms, termed symbionts, can fo ...

of ''R. pachyptila'' is capable of producing ATP by means of sulfide oxidation, and that ATP energy could be used to fix

carbon dioxide Carbon dioxide is a chemical compound with the chemical formula . It is made up of molecules that each have one carbon atom covalent bond, covalently double bonded to two oxygen atoms. It is found in a gas state at room temperature and at norma ...

Glycogen storage in trophosome

In ''

'', the

content of 100 μmol glycosyl units g⁻¹ fresh wt determined in the trophosome is divided equally between host and symbionts. Although the symbionts take up only 25% of the trophosome,

content is distributed equally between both partners, and this ratio remains similar for up to 40 h of hypoxia. Thus, host and symbiont each contain about 50 μmol glycosyl units g⁻¹ fresh wt of trophosome. This amount is comparable to that in other host tissues of ''R. pachyptila'', e.g. in the body wall (35 μmol glycosyl units g⁻¹ fresh wt) or the vestimentum (20 μmol glycosyl units g⁻¹ fresh wt), to that of other chemoautotrophic symbiotic animals and to that of nonsymbiotic animals known to be adapted to long-term anoxic periods.

Host-microbe interaction

Protection against oxidative damage

Higher concentration of

oxygen Oxygen is a chemical element; it has chemical symbol, symbol O and atomic number 8. It is a member of the chalcogen group (periodic table), group in the periodic table, a highly reactivity (chemistry), reactive nonmetal (chemistry), non ...

in the trophosome, (partial)

anaerobic metabolism Anaerobic respiration is respiration using electron acceptors other than molecular oxygen (O2). Although oxygen is not the final electron acceptor, the process still uses a respiratory electron transport chain. In aerobic organisms undergoing ...

of the host, and host

ROS Ros or ROS or RoS may refer to: Organizations * Raggruppamento Operativo Speciale, the Anti-organized Crime Branch of the Italian Carabinieri * Registers of Scotland, a Scottish authority responsible for compiling and maintaining records * Repart ...

-detoxifying

enzyme An enzyme () is a protein that acts as a biological catalyst by accelerating chemical reactions. The molecules upon which enzymes may act are called substrate (chemistry), substrates, and the enzyme converts the substrates into different mol ...

s in this tissue will not only shield the symbionts from

oxidative Redox ( , , reduction–oxidation or oxidation–reduction) is a type of chemical reaction in which the oxidation states of the reactants change. Oxidation is the loss of electrons or an increase in the oxidation state, while reduction is ...

damage but also minimize competition between the host and its oxygen symbionts.

Symbiont population control

Symbiont population control can be largely the result of symbiont

, which essentially prevents symbionts from escaping from their compartments and/or overgrowing the host. Nevertheless, the

immune system The immune system is a network of biological systems that protects an organism from diseases. It detects and responds to a wide variety of pathogens, from viruses to bacteria, as well as Tumor immunology, cancer cells, Parasitic worm, parasitic ...

can incorporate in phage defence and symbiont recognition during symbiosis.

Communication between host and microbe

The host communication may be involving the

eukaryote The eukaryotes ( ) constitute the Domain (biology), domain of Eukaryota or Eukarya, organisms whose Cell (biology), cells have a membrane-bound cell nucleus, nucleus. All animals, plants, Fungus, fungi, seaweeds, and many unicellular organisms ...

-like protein structure. These symbiont proteins which number more than 100 in the trophosome samples suggest a symbiotic-relevant role. Ankyrin repeats were believed to assist in the protein-protein interactions. The

ankyrin repeat The ankyrin repeat is a 33-residue motif in proteins consisting of two alpha helices separated by loops, first discovered in signaling proteins in yeast Cdc10 and '' Drosophila'' Notch. Domains consisting of ankyrin tandem repeats mediate ...

proteins could interact directly with the host proteins in order to modulate

endosome Endosomes are a collection of intracellular sorting organelles in eukaryotic cells. They are parts of the endocytic membrane transport pathway originating from the trans Golgi network. Molecules or ligands internalized from the plasma membra ...

maturation and interfere with host symbiont

References

External links

Pbs.org
{{Self-replicating organic structures Sabellida Protostome anatomy