Marine microbial symbiosis

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Possible ecological interactions between two individuals. The result of the interaction for each member of the pair can be positive, negative or neutral. For example, in predation, one partner obtains the benefits while the other assumes the costs. Ecological interactions between two individuals.png
Possible ecological interactions between two individuals. The result of the interaction for each member of the pair can be positive, negative or neutral. For example, in predation, one partner obtains the benefits while the other assumes the costs.

Microbial symbiosis in marine animals was not discovered until 1981. [3] In the time following, symbiotic relationships between marine invertebrates and chemoautotrophic bacteria have been found in a variety of ecosystems, ranging from shallow coastal waters to deep-sea hydrothermal vents. Symbiosis is a way for marine organisms to find creative ways to survive in a very dynamic environment. They are different in relation to how dependent the organisms are on each other or how they are associated. It is also considered a selective force behind evolution in some scientific aspects. The symbiotic relationships of organisms has the ability to change behavior, morphology and metabolic pathways. With increased recognition and research, new terminology also arises, such as holobiont, which the relationship between a host and its symbionts as one grouping. [4] Many scientists will look at the hologenome, which is the combined genetic information of the host and its symbionts. These terms are more commonly used to describe microbial symbionts.

Contents

The type of marine animal vary greatly, for example, sponges, sea squirts, corals, worms, and algae all host a variety of unique symbionts. [5] Each symbiotic relationship displays a unique ecological niche, which in turn can lead to entirely new species of host species and symbiont. [3]

It is particularly interesting that it took so long to discover the marine microbial symbiosis because nearly every surface submerged in the oceans becomes covered with biofilm, [6] including a large number of living organisms. Many marine organisms display symbiotic relationships with microbes. Epibiotic bacteria have been found to live on crustacean larvae and protect them from fungal infections. [6] Other microbes in deep-sea vents have been found to prevent the settlement of barnacles and tunicate larvae. [6]

Mechanisms of symbiosis

Various mechanisms are utilized in order to facilitate symbiotic relationships and to help these associates evolve alongside one another. By using horizontal gene transfer, certain genetic elements are able to pass from one organisms to another. In non-mating species, this helps with genetic differentiation and adaptive evolution. [7] An example of this is the sponge Astroclera willeyana which has a gene that is used in expressing spherulite-forming cells which has an origin in bacteria. Another example is the starlet sea anemone, Nematostella vectensis, which has genes from bacteria that have a role in producing UV radiation protection in the form of shikimic acid. Another way for symbiotic relationships to co-evolve is through genome erosion. This is a process where genes that are typically used during free-living periods aren't necessary because of the symbioses of the organisms. Without that gene, the organism is able to decrease the energy necessary for cell maintenance and replication. [7]

Types of symbiotic relationships

Main types of microbial symbioses (A) Microbial interactions range from mutually beneficial to harmful for one or more partners. Blue double headed arrows highlight that relationships can move between classifications often influenced by environmental conditions. (B) Host-microbe symbioses should be considered within the context of microbial communities where the host participates in multiple and often different symbiotic relationships. (C) Microbial communities are influenced by a variety of microbe-microbe symbioses ranging from cooperation (e.g., syntrophy or co-metabolism) to competition. Arrows depict generally beneficial (blue) and detrimental (red) outcomes for one (single arrowhead) or both (double arrowhead) members. Note as with host-microbe symbioses these relationships can be viewed as fluid and influenced by environmental conditions. Types of microbial symbioses.jpg
Main types of microbial symbioses
(A) Microbial interactions range from mutually beneficial to harmful for one or more partners. Blue double headed arrows highlight that relationships can move between classifications often influenced by environmental conditions. (B) Host-microbe symbioses should be considered within the context of microbial communities where the host participates in multiple and often different symbiotic relationships. (C) Microbial communities are influenced by a variety of microbe-microbe symbioses ranging from cooperation (e.g., syntrophy or co-metabolism) to competition. Arrows depict generally beneficial (blue) and detrimental (red) outcomes for one (single arrowhead) or both (double arrowhead) members. Note as with host-microbe symbioses these relationships can be viewed as fluid and influenced by environmental conditions.

There are a variety of symbiotic relationships:

The relationship can be either an ectosymbiont, a symbiont that survives by being attached to the surface of the host, which includes areas such as the inner surfaces of the gut cavity, or even the ducts of endocrine glands; or an endosymbiont, a symbiont that lives within its host and can be known as an intracellular symbiont. [7]

They are further classified by their dependence on their host and can be a facultative symbiont that can exist in a free living condition and is not dependent on its host, or an obligate symbiont, which has adapted in such a way that it is not able to exit without the benefit it receives from its host. An example of an obligate symbioses is the relationship between microalgae and corals. The microalgae provides a large source of the coral diet [7]

Some symbiotic relationships

Coral reef symbiosis

The most notable display of marine symbiotic relationship would be coral. Coral reefs are home to a variety of dinoflagellate symbiont, [10] these symbionts give coral its bright coloring and are vital for the survival of the reef. The symbionts provide the coral with food in exchange for protection. If the waters warm or become too acidic, the symbionts are expelled, the coral bleaches and if conditions persist the coral will die. This in turn leads to the collapse of the entire reef ecosystem [10]

Bone eating worm symbiosis

Figure 1 shows Osedax rubiplumus with ovisac (red colored projections) which houses symbiont bacteria Osedax rubiplumus.jpg
Figure 1 shows Osedax rubiplumus with ovisac (red colored projections) which houses symbiont bacteria

Osedax, also called the bone eating worm is a siboglinid worm from polychaete genus. It was discovered in a whalefall community on the surface of bones, in the axis of Monterey Canyon, California, in 2002. Osedax lacks a mouth, a functional gut and a trophosome. But female osedax have a vascularized root system originating from their ovisac which contains heterotrophic endosymbiotic bacterial community dominated by γ-proteobacteria clade. They use the vascularized root system to access the whale bones. The endosymbionts help the host utilize nutrients from the whale bones. [11]

Hawaiian squid and Vibrio fischeri symbiosis

Hawaiian sepiolid squid Euprymna scolopes and bacterium Vibrio fischeri also show symbiosis. In this symbiosis, symbiont not only serve the host for defense, but also shapes the host morphology. Bioluminescent V. fischeri can be found in epithelial lined crypts of the light organ of the host. Symbiosis begins as soon as a newly hatched squid finds and houses V. fischeri bacteria.

Figure 2 shows sagittal section of bobtail squid Euprymna scolopes. light organ. The crypts house symbiont bacteria Vibrio fischeri. They emit light during night time to camouflage themselves against the moon and star light coming down the ocean. It helps them to avoid predators. Bobtail Squid Light Organ.svg
Figure 2 shows sagittal section of bobtail squid Euprymna scolopes. light organ. The crypts house symbiont bacteria Vibrio fischeri. They emit light during night time to camouflage themselves against the moon and star light coming down the ocean. It helps them to avoid predators.

The symbiosis process begins when Peptidoglycan shed by the sea water bacteria comes in contact to the ciliated epithelial cells of the light organ. It induces mucus production in the cells. Mucus entraps bacterial cells. Antimicrobial peptides, nitric oxide and sialyted mucins in the mucus then selectively allow only V. fischeri which encode gene rscS to adhere and win over gram positive and other gram negative bacteria. The symbiotic bacteria are then guided up to the light organ via chemotaxis. After successful colonization, symbionts induce loss of mucus and ciliated sites to prevent further attachment of bacterial cells via MAMP (microbe associated molecular pattern) signalling. Also, they induce changes in protein expression in the host symbiotic tissues and modify both physiology and morphology of light organs. After bacterial cells divide and increase in population, they begin expressing enzyme luciferase as a result of quorum sensing. Luciferase enzymes produce bioluminescence. [12] Squids can then emit the luminescence from the light organ. Because Euprymna scolopes emerges only during night time, it helps them avoid predation. Bioluminescence allows them to camouflage with the light coming from moon and stars to ocean and avoid predators. [13]

Pompeii worm

Alvinella pompejana, the Pompeii worm is a polychaete, found in the far depths of the sea, typically found near hydrothermal vents. They were originally discovered by French researchers in the early 1980s. [14] They can grow as large as 5 inches long and are normally described as having pale gray coloring with red "tentacle-like" gills protruding from their heads. Their tails are most likely found in temperatures as high as 176 degrees Fahrenheit, while their heads, which stick out from the tubes they live in are only exposed to temperatures as high as 72 degrees Fahrenheit. [14] Its ability to survive the temperatures of hydrothermal vents lies in its symbiotic relationship with the bacteria that resides on its back. It forms a "fleece-like" protective covering. Mucus is secreted from glands on the back of the Pompeii worm in order to provide nutrients for the bacteria. Further study of the bacteria led to the discovery that they are chemolithotrophic. [14]  

Hawaiian sea slug

Elysia rufescens grazes on Bryopsis sp., an alga that defends itself from predators by using peptide toxins with fatty acids, called kahalalides. [15] A bacterial obligate symbiont produces many defensive molecules, including kahalalides, in order to protect the alga. This bacteria is able to use substrates derived from the host in order to synthesize the toxins. [15] The Hawaiian Sea Slug grazes on the alga in order to accumulate kahalalide. This uptake of the toxin, which the slug is immune to, allows it to also become toxic to predators. This shared ability, both originating from the bacteria, provide protection within the marine ecosystems.

Marine sponges

The sponge holobiont The sponge holobiont is an example of the concept of nested ecosystems. Key functions carried out by the microbiome (coloured arrows) influence holobiont functioning and, through cascading effects, subsequently influence community structure and ecosystem functioning. Environmental factors act at multiple scales to alter microbiome, holobiont, community, and ecosystem scale processes. Thus, factors that alter microbiome functioning can lead to changes at the holobiont, community, or even ecosystem level and vice versa, illustrating the necessity of considering multiple scales when evaluating functioning in nested ecosystems. DOM: dissolved organic matter; POM: particulate organic matter; DIN: dissolved inorganic nitrogen The sponge holobiont.webp
The sponge holobiont
The sponge holobiont is an example of the concept of nested ecosystems. Key functions carried out by the microbiome (coloured arrows) influence holobiont functioning and, through cascading effects, subsequently influence community structure and ecosystem functioning. Environmental factors act at multiple scales to alter microbiome, holobiont, community, and ecosystem scale processes. Thus, factors that alter microbiome functioning can lead to changes at the holobiont, community, or even ecosystem level and vice versa, illustrating the necessity of considering multiple scales when evaluating functioning in nested ecosystems.
DOM: dissolved organic matter; POM: particulate organic matter; DIN: dissolved inorganic nitrogen

Besides a one to one symbiotic relationship, it is possible for a host to become symbiotic with a microbial consortia. In the case of the sponge (phylum Porifera), they are able to host a lot of wide range of microbial communities that can also be very specific. The microbial communities that form a symbiotic relationship with the sponge can actually comprise up to 35% of the biomass of its host. [17] The term for this specific symbiotic relationship, where a microbial consortia pairs with a host is called a holobiotic relationship. The sponge as well as the microbial community associated with it will produce a large range of secondary metabolites that help protect it against predators through mechanisms such as chemical defense. [18] Some of these relationships include endosymbionts within bacteriocyte cells, and cyanobacteria or microalgae found below the pinacoderm cell layer where they are able to receive the highest amount of light, used for phototrophy. They can host approximately 52 different microbial phyla and candidate phyla, including Alphaproteobacteria, Actinobacteria, Chloroflexi, Nitrospirae, Cyanobacteria, the taxa Gamma-, and the candidate phylum Poribacteria, and Thaumarchaea. [18]

Endozoicomonas

This type of bacteria was first described in 2007. [19] It is able to form symbiotic relationships with a wide range of hosts in the marine environment such as cnidarians, poriferans, molluscs, annelids, tunicates, and fish. They are distributed through various marine zones from extreme depths to warm photic zones. Endozoicomonas is thought to acquisition nutrients from nitrogen/carbon recycling, methane/sulfur recycling, and synthesize amino acids and various other molecules necessary for life. [19] It was also found that it has a correlation to photosymbionts which provide carbon and sulfur to the bacteria from dimethylsulfopropionate (DMSP). They are also suspected to help regulate bacterial colonization of the host by using bioactive secondary metabolites or even probiotic mechanisms like limiting pathogenic bacteria by means of competitive exclusion. When Endozoicomonas is removed from the host, there are often signs of lesions on corals and disease. [19]

Chemosynthetic symbioses in ocean

Marine environment consists of a large number of chemosynthetic symbioses in different regions of the ocean: shallow-water coastal sediments, continental slope sediments, whale and wood falls, cold seeps and deep-sea hydrothermal vents. Organisms from seven phyla (ciliophora, porifera, platyhelminthes, nematoda, mollusca, annelida and arthropoda) are known to have chemosynthetic symbiosis till now. Some of them include nematode, tube worms, clam, sponge, hydrothermal vent shrimp, worms mollusc, mussels and so on. The symbionts can be ectosymbionts or endosymbionts. Some ectosymbionts are: symbionts of polychaete worm Alvinella which occur in their dorsal surface and symbionts occurring on the mouthparts and gill chamber of the vent shrimp Rimicaris. Endosymbionts include symbionts of gastropod snails which occur in their gill tissues. In the siboglinid tube worms of the groups Monilifera, Frenulata and Vestimentifera, symbionts can be found in an interior organ called trophosome. [20]

Most of the animals in deep-sea hydrothermal vents exist in a symbiotic relationship with chemosynthetic bacteria. These chemosynthetic bacteria are found to be methane or sulphur oxidizers.   [21]

Microbial biotechnology

Marine invertebrates are the hosts of a wide spectrum of bioactive metabolites, which have vast potential as drugs and research tools. [22] In many cases, microbes aid in or are responsible for marine invertebrates natural products. [22] Certain marine microbes can provide insight into the biosynthesis mechanisms of natural products, which in turn could solve the current limitations on marine drug development. [5]

Related Research Articles

<span class="mw-page-title-main">Endosymbiont</span> Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is an organism that lives within the body or cells of another organism. Typically the two organisms are in a mutualistic relationship. Examples are nitrogen-fixing bacteria, which live in the root nodules of legumes, single-cell algae inside reef-building corals, and bacterial endosymbionts that provide essential nutrients to insects.

<span class="mw-page-title-main">Symbiosis</span> Close, long-term biological interaction between distinct organisms (usually species)

Symbiosis is any type of a close and long-term biological interaction, between two organisms of different species. The two organisms, termed symbionts, can be either in a mutualistic, a commensalistic, or a parasitic relationship. In 1879, Heinrich Anton de Bary defined symbiosis as "the living together of unlike organisms".

<i>Riftia</i> Giant tube worm (species of annelid)

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 related to tube worms commonly found in the intertidal and pelagic zones. R. pachyptila lives on the floor of the Pacific Ocean near hydrothermal vents. The vents provide a natural ambient temperature in their environment ranging from 2 to 30 °C, and this organism can tolerate extremely high hydrogen sulfide levels. These worms can reach a length of 3 m, and their tubular bodies have a diameter of 4 cm (1.6 in).

Symbiotic bacteria are bacteria living in symbiosis with another organism or each other. For example, rhizobia living in root nodules of legumes provide nitrogen fixing activity for these plants.

Horizontal transmission is the transmission of organisms between biotic and/or abiotic members of an ecosystem that are not in a parent-progeny relationship. Because the evolutionary fate of the agent is not tied to reproductive success of the host, horizontal transmission tends to evolve virulence. It is therefore a critical concept for evolutionary medicine.

<span class="mw-page-title-main">Gammaproteobacteria</span> Class of bacteria

Gammaproteobacteria is a class of bacteria in the phylum Pseudomonadota. It contains about 250 genera, which makes it the most genus-rich taxon of the Prokaryotes. Several medically, ecologically, and scientifically important groups of bacteria belong to this class. All members of this class are Gram-negative. It is the most phylogenetically and physiologically diverse class of the Pseudomonadota.

Cyanobionts are cyanobacteria that live in symbiosis with a wide range of organisms such as terrestrial or aquatic plants; as well as, algal and fungal species. They can reside within extracellular or intracellular structures of the host. In order for a cyanobacterium to successfully form a symbiotic relationship, it must be able to exchange signals with the host, overcome defense mounted by the host, be capable of hormogonia formation, chemotaxis, heterocyst formation, as well as possess adequate resilience to reside in host tissue which may present extreme conditions, such as low oxygen levels, and/or acidic mucilage. The most well-known plant-associated cyanobionts belong to the genus Nostoc. With the ability to differentiate into several cell types that have various functions, members of the genus Nostoc have the morphological plasticity, flexibility and adaptability to adjust to a wide range of environmental conditions, contributing to its high capacity to form symbiotic relationships with other organisms. Several cyanobionts involved with fungi and marine organisms also belong to the genera Richelia, Calothrix, Synechocystis, Aphanocapsa and Anabaena, as well as the species Oscillatoria spongeliae. Although there are many documented symbioses between cyanobacteria and marine organisms, little is known about the nature of many of these symbioses. The possibility of discovering more novel symbiotic relationships is apparent from preliminary microscopic observations.

<span class="mw-page-title-main">Trophosome</span> Organ containing endosymbionts

A trophosome is a highly vascularised organ found in some animals that houses symbiotic bacteria that provide food for their host. Trophosomes are contained by the coelom of tube worms and in the body of symbiotic flatworms of the genus Paracatenula.

The hologenome theory of evolution recasts the individual animal or plant as a community or a "holobiont" – the host plus all of its symbiotic microbes. Consequently, the collective genomes of the holobiont form a "hologenome". Holobionts and hologenomes are structural entities that replace misnomers in the context of host-microbiota symbioses such as superorganism, organ, and metagenome. Variation in the hologenome may encode phenotypic plasticity of the holobiont and can be subject to evolutionary changes caused by selection and drift, if portions of the hologenome are transmitted between generations with reasonable fidelity. One of the important outcomes of recasting the individual as a holobiont subject to evolutionary forces is that genetic variation in the hologenome can be brought about by changes in the host genome and also by changes in the microbiome, including new acquisitions of microbes, horizontal gene transfers, and changes in microbial abundance within hosts. Although there is a rich literature on binary host–microbe symbioses, the hologenome concept distinguishes itself by including the vast symbiotic complexity inherent in many multicellular hosts.

<i>Olavius algarvensis</i> Species of annelid worm

Olavius algarvensis is a species of gutless oligochaete worm in the family Tubificidae which depends on symbiotic bacteria for its nutrition.

<i>Paracatenula</i> Genus of flatworms

Paracatenula is a genus of millimeter sized free-living marine gutless catenulid flatworms.

<span class="mw-page-title-main">Holobiont</span> Host and associated species living as a discrete ecological unit

A holobiont is an assemblage of a host and the many other species living in or around it, which together form a discrete ecological unit through symbiosis, though there is controversy over this discreteness. The components of a holobiont are individual species or bionts, while the combined genome of all bionts is the hologenome. The holobiont concept was initially introduced by the German theoretical biologist Adolf Meyer-Abich in 1943, and then apparently independently by Dr. Lynn Margulis in her 1991 book Symbiosis as a Source of Evolutionary Innovation. The concept has evolved since the original formulations. Holobionts include the host, virome, microbiome, and any other organisms which contribute in some way to the functioning of the whole. Well-studied holobionts include reef-building corals and humans.

Hologenomics is the omics study of hologenomes. A hologenome is the whole set of genomes of a holobiont, an organism together with all co-habitating microbes, other life forms, and viruses. While the term hologenome originated from the hologenome theory of evolution, which postulates that natural selection occurs on the holobiont level, hologenomics uses an integrative framework to investigate interactions between the host and its associated species. Examples include gut microbe or viral genomes linked to human or animal genomes for host-microbe interaction research. Hologenomics approaches have also been used to explain genetic diversity in the microbial communities of marine sponges.

Stilbonematinae is a subfamily of the nematode worm family Desmodoridae that is notable for its symbiosis with sulfur-oxidizing bacteria.

<span class="mw-page-title-main">Hydrothermal vent microbial communities</span> Undersea unicellular organisms

The hydrothermal vent microbial community includes all unicellular organisms that live and reproduce in a chemically distinct area around hydrothermal vents. These include organisms in the microbial mat, free floating cells, or bacteria in an endosymbiotic relationship with animals. Chemolithoautotrophic bacteria derive nutrients and energy from the geological activity at Hydrothermal vents to fix carbon into organic forms. Viruses are also a part of the hydrothermal vent microbial community and their influence on the microbial ecology in these ecosystems is a burgeoning field of research.

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

All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal–microbial relationships were historically explored in single host–symbiont systems. However, new explorations into the diversity of marine microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and a more multi-member microbiome. The potential for microbiomes to influence the health, physiology, behavior, and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment.

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

The holobiont concept is a renewed paradigm in biology that can help to describe and understand complex systems, like the host-microbe interactions that play crucial roles in marine ecosystems. However, there is still little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them and their ecological consequences. The holobiont concept posits that a host and its associated microbiota with which it interacts, form a holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution.

Hydrogen sulfide chemosynthesis is a form of chemosynthesis which uses hydrogen sulfide. It is common in hydrothermal vent microbial communities Due to the lack of light in these environments this is predominant over photosynthesis

Oligobrachia is a genus in the family Siboglinidae, commonly known as beard worms. These beard worms are typically found at spreading centers, hydrothermal vents, and undersea volcanoes. The siboglinidae are annelids which can be found buried in sediments. Beard worms do not necessarily exist at one specific part of the world's oceans, however, they are spread out all over the ocean floors as long as the surrounding environment is similar; these are known as metapopulations. Most commonly, these organisms are found at the bottom of the ocean floor, whether it be at a depth of roughly 25 meters or hundreds of meters. Oligobrachia can typically be found near hydrothermal vents and methane seeps. An important characteristic of this genus is that it lacks a mouth and gut. Therefore, it relies on symbiotic bacteria to provide the host organism with energy to survive. The majority of oligobrachia that have been observed have been found in the Arctic and other high-latitude areas of the world's oceans.

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

Sponge microbiomes are diverse communities of microorganisms in symbiotic association with marine sponges as their hosts. These microorganisms include bacteria, archaea, fungi, viruses, among others. The sponges have the ability to filter seawater and recycle nutrients while providing a safe habitat to many microorganisms, which provide the sponge host with fixed nitrogen and carbon, and stimulates the immune system. Together, a sponge and its microbiome form a holobiont, with a single sponge often containing more than 40 bacterial phyla, making sponge microbial environments a diverse and dense community. Furthermore, individual holobionts work hand in hand with other near holobionts becoming a nested ecosystem, affecting the environment at multiple scales.

References

  1. ↑ Faust K and Raes J (2012) "Microbial interactions: From networks to models". Nat Rev Microbiol, 10: 538–550. doi : 10.1038/nrmicro2832.
  2. ↑ Krabberød, A.K., Bjorbækmo, M.F., Shalchian-Tabrizi, K. and Logares, R. (2017) "Exploring the oceanic microeukaryotic interactome with metaomics approaches". Aquatic Microbial Ecology, 79(1): 1–12. doi : 10.3354/ame01811. CC-BY icon.svg Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
  3. 1 2 Cavanaugh CM (February 1994). "Microbial Symbiosis: Patterns of Diversity in the Marine Environment". American Zoologist. 34 (1): 79–89. doi: 10.1093/icb/34.1.79 . JSTOR   3883820.
  4. ↑ Egan S, Gardiner M (2016). "Microbial Dysbiosis: Rethinking Disease in Marine Ecosystems". Frontiers in Microbiology. 7: 991. doi: 10.3389/fmicb.2016.00991 . PMC   4914501 . PMID   27446031.
  5. 1 2 Li Z (April 2009). "Advances in marine microbial symbionts in the china sea and related pharmaceutical metabolites". Marine Drugs. 7 (2): 113–29. doi: 10.3390/md7020113 . PMC   2707038 . PMID   19597576.
  6. 1 2 3 Armstrong E, Yan L, Boyd KG, Wright PC, Burgess JG (October 2001). "The symbiotic role of marine microbes on living surfaces". Hydrobiologia. 461 (1–3): 37–40. doi:10.1023/A:1012756913566. S2CID   33165122.
  7. 1 2 3 4 Apprill A (January 2020). "The Role of Symbioses in the Adaptation and Stress Responses of Marine Organisms". Annual Review of Marine Science. 12 (1): 291–314. Bibcode:2020ARMS...12..291A. doi: 10.1146/annurev-marine-010419-010641 . PMID   31283425.
  8. ↑ Egan, S., Fukatsu, T. and Francino, M.P., 2020. Opportunities and Challenges to Microbial Symbiosis Research in the Microbiome Era. Frontiers in Microbiology, 11. doi : 10.3389/fmicb.2020.01150. CC-BY icon.svg Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
  9. ↑ Fukui S (May 2014). "Evolution of symbiosis with resource allocation from fecundity to survival". Die Naturwissenschaften. 101 (5): 437–46. Bibcode:2014NW....101..437F. doi:10.1007/s00114-014-1175-1. PMC   4012156 . PMID   24744057.
  10. 1 2 Baker A (November 2003). "Flexibility and Specificity in Coral-Algal Symbiosis: Diversity, Ecology, and Biogeography of Symbiodinium". Annual Review of Ecology, Evolution, and Systematics. 34: 661–689. doi:10.1146/annurev.ecolsys.34.011802.132417. JSTOR   30033790.
  11. ↑ Goffredi SK, Orphan VJ, Rouse GW, Jahnke L, Embaye T, Turk K, et al. (September 2005). "Evolutionary innovation: a bone-eating marine symbiosis". Environmental Microbiology. 7 (9): 1369–78. doi:10.1111/j.1462-2920.2005.00824.x. PMID   16104860.
  12. ↑ Schwartzman JA, Ruby EG (January 2016). "A conserved chemical dialog of mutualism: lessons from squid and vibrio". Microbes and Infection. 18 (1): 1–10. doi:10.1016/j.micinf.2015.08.016. PMC   4715918 . PMID   26384815.
  13. ↑ Nyholm SV, McFall-Ngai MJ (August 2004). "The winnowing: establishing the squid-vibrio symbiosis". Nature Reviews. Microbiology. 2 (8): 632–42. doi:10.1038/nrmicro957. PMID   15263898. S2CID   21583331.
  14. 1 2 3 "Pompeii Worm". Marine Symbiosis. Retrieved 2020-04-29.
  15. 1 2 Zan J, Li Z, Tianero MD, Davis J, Hill RT, Donia MS (June 2019). "A microbial factory for defensive kahalalides in a tripartite marine symbiosis". Science. 364 (6445): eaaw6732. doi:10.1126/science.aaw6732. PMID   31196985. S2CID   189818260.
  16. ↑ Pita, L., Rix, L., Slaby, B.M., Franke, A. and Hentschel, U. (2018) "The sponge holobiont in a changing ocean: from microbes to ecosystems". Microbiome, 6(1): 46. doi : 10.1186/s40168-018-0428-1. CC-BY icon.svg Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
  17. ↑ Egan S, Thomas T (2015). "Editorial for: Microbial symbiosis of marine sessile hosts- diversity and function". Frontiers in Microbiology. 6: 585. doi: 10.3389/fmicb.2015.00585 . PMC   4468920 . PMID   26136729.
  18. 1 2 Webster NS, Thomas T (April 2016). "The Sponge Hologenome". mBio. 7 (2): e00135-16. doi:10.1128/mBio.00135-16. PMC   4850255 . PMID   27103626.
  19. 1 2 3 Neave MJ, Apprill A, Ferrier-Pagès C, Voolstra CR (October 2016). "Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas". Applied Microbiology and Biotechnology. 100 (19): 8315–24. doi:10.1007/s00253-016-7777-0. PMC   5018254 . PMID   27557714.
  20. ↑ Dubilier N, Bergin C, Lott C (October 2008). "Symbiotic diversity in marine animals: the art of harnessing chemosynthesis". Nature Reviews. Microbiology. 6 (10): 725–40. doi:10.1038/nrmicro1992. PMID   18794911. S2CID   3622420.
  21. ↑ Petersen JM, Zielinski FU, Pape T, Seifert R, Moraru C, Amann R, et al. (August 2011). "Hydrogen is an energy source for hydrothermal vent symbioses". Nature. 476 (7359): 176–80. Bibcode:2011Natur.476..176P. doi:10.1038/nature10325. PMID   21833083. S2CID   25578.
  22. 1 2 Haygood MG, Schmidt EW, Davidson SK, Faulkner DJ (August 1999). "Microbial symbionts of marine invertebrates: opportunities for microbial biotechnology" (PDF). Journal of Molecular Microbiology and Biotechnology. 1 (1): 33–43. PMID   10941782.
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