Fungal-bacterial endosymbiosis

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Fungal-bacterial endosymbiosis encompasses the mutualistic relationship between a fungus and intracellular bacteria species residing within the fungus. Many examples of endosymbiotic relationships between bacteria and plants, algae and insects exist and have been well characterized, however fungal-bacteria endosymbiosis has been less well described.

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Fungal-bacterial endosymbiosis represents a diverse range of endosymbionts and hosts with respect to the initiation of the association and the benefits provided by and for each partner. Well-studied examples include Burkholderia species (sp.)/Rhizopus microsporus (R. microsporus), Nostoc punctiforme (N. punctiforme)/Geosiphon pyriforme (G. pyriforme) [1] [2] and Candidatus Glomeribacter gigasporarum (Ca. G. sporarum) /Gigaspora margarita (G. margarita) bacteria/fungi associations. What is known on these associations impacts our understanding of the ecological interactions of plants, fungi and bacteria.

Taxonomy

The classification of bacterial endosymbionts and their fungal partners occur across a diverse set of phyla. Ca. G. sporarum and Burkholderia sp. have been identified to be β-proteobacteria, a gram-negative class of bacteria, and N. punctiforme is a cyanobacteria . These phyla are not closely related showing that the capability of endosymbiosis with fungi is widely spread. A similar pattern is seen with the fungal partners with examples occurring across broad phyla/divisions such as Glomeromycota, Zygomycota, Ascomycota and Basidiomycota. The common feature of these fungi is that they are often arbuscular or ectomycorrhizal fungi and form symbiotic relations with plants as well as with their bacterial endosymbionts. Though commonalities exist, the taxonomic classification does not offer a consistent symbiotic phenotype.

Morphology

The definition of “endosymbiont” indicates that the bacteria are localized within the cytoplasm of cells or hyphae of the fungi partner. Specifically, the bacteria grow within the membranes of their fungal counterpart, commonly referred to as vacuoles or symbiosomes. This is a feature common in all fungal-bacterial symbiosis suggesting that internalization of the bacteria via phagocytosis is the main method of incorporation.

Life cycles

The bacteria involved may be internalized by the fungi on a cyclic basis or obligatorily living within the fungi. The interaction between N. punctiforme and G. pyriforme is an example of a cyclical association which forms at a certain point in their separate life cycles. N. punctiforme forms masses of filaments which gather in the dimmer underground soil while G. pyriforme grows lateral vegetative hyphae occupying the same area. The endosymbiotic relationship is formed when G. pyriforme engulf and internalize N. punctiforme in their growing hyphae in specialized compartments. Within the fungi, N. punctiforme replicates for the duration of about 6 months, coinciding with the life span of Geosiphon. Ca. G. sporarum, in contrast, is an obligate endosymbiont in the AM (arbuscular mycorrhizal) fungus G. margarita. They have been observed replicating within vacuoles and have been found in all stages of the life of the fungus including the spores, vegetative hyphae, and plant cell-associated hyphae. It is thought that the bacteria are transmitted vertically from parent to offspring in the fungi as permanent residents. Thus, bacterial endosymbionts are typically incorporated into growing fungi either through phagocytosis during some point in the life cycle of the fungus or passed on vertically forming permanent associations with the fungus.

Benefits and metabolism

In most cases, bacteria provide the fungus with some form of metabolic benefit while the fungus often provides a suitable living environment. Burkholderia sp. in R. microsporus have been found to produce rhizoxin, an inhibitor of mitosis originally thought to be produced by R. microsporus itself. The production of rhizoxin by Burkholderia sp. leading to the death of plant cells allows R. microsporus to gain greater access to nutrients. The bacteria also appears to play a role in dictating asexual spore formation in R. microsporus. The benefit gained by the bacteria in this case is not specifically known. In other cases such as N. punctiforme and Ca. G. sporarum, nutrient exchange exists between the partners. N. punctiforme are autotrophic cyanobacteria capable of fixing nitrogen and provides G. pyriforme with fixed nitrogen. Ca. G. sporarum, on the other hand, has been found to increase the content of fatty acids, a method of usable organic carbon storage, in G. margarita while relying heavily on its AM fungi host to provide key nutrients suggesting that nutrient exchange is a two-way interaction. The AM fungi host relies on the plant host for its nutrients. Interactions between bacteria and fungi are based on benefits to metabolism and represent complex interactions between bacterial, fungal and plant components.

Applications and significance

Many of the fungal partners involved in the endosymbiotic relationship with the bacteria are also in mutualistic or parasitic relationships with other plants. The presence of intracellular bacteria living within these fungi add another level of complexity and suggests that at some level, the plant is benefitting indirectly from the interaction between fungi and bacteria. About 80% of natural and cultivated plants harbour AM fungi. These interactions increase nutrient availability in the plant and lead to increased plant growth and environmental stress-resistance. There exists a current demand in agriculture to cultivate and optimize to increase yield sustainably. Without considering the bacteria that live within AM fungi, like Ca. G. sporarum, as a factor that may contribute the beneficial nature of AM fungi to plants, we may overlook what makes widespread agricultural application possible. On the other side of the spectrum are the fungi that cause disease in agricultural crops leading to huge loses, such as R. microsporus which causes blight in rice seedlings. R. microsporus relies on its bacterial partner of the Burkholderia sp. for the pathogenic toxin. Previous efforts to control infection included the use of harmful pesticides to eliminate the fungi, however more recent research takes into mind the role of the endosymbiotic bacteria in pathogenesis and uses phages to target the bacteria. We can see that fungal-bacterial endosymbiosis significantly impacts the global concern of food production and we can think of the deeper understanding of these relationships as being the solution to these problems.

Related Research Articles

Endosymbiont Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is any organism that lives within the body or cells of another organism most often, though not always, in a mutualistic relationship. (The term endosymbiosis is from the Greek: ἔνδον endon "within", σύν syn "together" and βίωσις biosis "living".) 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 about 10–15% of insects.

Symbiosis Type of a close and long-term biological interaction between two different biological organisms

Symbiosis is any type of a close and long-term biological interaction between two different biological organisms, be it mutualistic, commensalistic, or parasitic. The organisms, each termed a symbiont, must be of different species. In 1879, Heinrich Anton de Bary defined it as "the living together of unlike organisms". The term was subject to a century-long debate about whether it should specifically denote mutualism, as in lichens. Biologists have now abandoned that restriction.

Mycorrhiza Symbiotic association between a fungus and the roots of a vascular plant

A mycorrhiza is a mutual symbiotic association between a fungus and a plant. The term mycorrhiza refers to the role of the fungus in the plant's rhizosphere, its root system. Mycorrhizae play important roles in plant nutrition, soil biology and soil chemistry.

Endophyte

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; however, most of the endophyte/plant relationships are not well understood. Some endophytes may enhance host growth, nutrient acquisition and improve the plant's ability to tolerate abiotic stresses, such as drought, salinity and decrease biotic stresses by enhancing plant resistance to insects, pathogens and herbivores.

Arbuscular mycorrhiza

An arbuscular mycorrhiza is a type of mycorrhiza in which the symbiont fungus penetrates the cortical cells of the roots of a vascular plant forming arbuscules.

Root hair

Root hairs, or absorbent hairs, are tubular outgrowths of a trichoblast, a hair-forming cell on the epidermis of a plant root. These structures are lateral extensions of a single cell and are only rarely branched. They are found in the region of maturation, also called the zone of differentiation of the root. Just prior to and during root hair cell development, there is elevated phosphorylase activity. Plants absorb water through the roots from the soil by bulk flow. Root hair cells are adapted to this process by increasing root surface area for the purpose of taking in more water. The large vacuole inside root hair cells makes this intake much more efficient.

Glomeromycota Phylum of fungi

Glomeromycota are one of eight currently recognized divisions within the kingdom Fungi, with approximately 230 described species. Members of the Glomeromycota form arbuscular mycorrhizas (AMs) with the thalli of bryophytes and the roots of vascular land plants. Not all species have been shown to form AMs, and one, Geosiphon pyriformis, is known not to do so. Instead, it forms an endocytobiotic association with Nostoc cyanobacteria. The majority of evidence shows that the Glomeromycota are dependent on land plants for carbon and energy, but there is recent circumstantial evidence that some species may be able to lead an independent existence. The arbuscular mycorrhizal species are terrestrial and widely distributed in soils worldwide where they form symbioses with the roots of the majority of plant species (>80%). They can also be found in wetlands, including salt-marshes, and associated with epiphytic plants.

Bacteriocyte

A bacteriocyte, also known as a mycetocyte, is a specialized adipocyte found primarily in certain insect groups such as aphids, tsetse flies, German cockroaches, weevils. These cells contain endosymbiotic organisms such as bacteria and fungi, which provide essential amino acids and other chemicals to their host. Bacteriocytes may aggregate into a specialized organ called the bacteriome.

<i>Geosiphon</i> Monotypic genus of photosynthetic, non-lichen fungi

Geosiphon is a genus of fungus in the family Geosiphonaceae. The genus is monotypic, containing the single species Geosiphon pyriformis, first described by Kützing in 1849 as Botrydium pyriforme. In 1915, Von Wettstein characterized Geosiphon pyriforme as a multinucleate alga containing endosymbiotic cyanobacteria, although he also noted the presence of chitin, a component of fungal cell walls. In 1933, Knapp was the first to suggest the fungal origin of the species and described it as a lichen with endosymbiotic cyanobacteria. It is the only member of the Glomeromycota known to not form a symbiosis with terrestrial plants in the form of arbuscular mycorrhiza.

Rhizoxin Chemical compound

Rhizoxin is an antimitotic agent with anti-tumor activity. It is isolated from a pathogenic plant fungus which causes rice seedling blight.

<i>Rhizopus microsporus</i> Species of fungus

Rhizopus microsporus is a fungal plant pathogen infecting maize, sunflower, and rice.

Fungivore Organism that consumes fungi

Fungivory or mycophagy is the process of organisms consuming fungi. Many different organisms have been recorded to gain their energy from consuming fungi, including birds, mammals, insects, plants, amoebas, gastropods, nematodes, bacteria and other fungi. Some of these, which only eat fungi, are called fungivores whereas others eat fungi as only part of their diet, being omnivores.

Nitrogen nutrition in the arbuscular mycorrhizal system refers to...

The mycorrhizosphere is the region around a mycorrhizal fungus in which nutrients released from the fungus increase the microbial population and its activities. The roots of most terrestrial plants, including most crop plants and almost all woody plants, are colonized by mycorrhiza-forming symbiotic fungi. In this relationship, the plant roots are infected by a fungus, but the rest of the fungal mycelium continues to grow through the soil, digesting and absorbing nutrients and water and sharing these with its plant host. The fungus in turn benefits by receiving photosynthetic sugars from its host. The mycorrhizosphere consists of roots, hyphae of the directly connected mycorrhizal fungi, associated microorganisms, and the soil in their direct influence.

Ectomycorrhiza

An ectomycorrhiza is a form of symbiotic relationship that occurs between a fungal symbiont, or mycobiont, and the roots of various plant species. The mycobiont is often from the phyla Basidiomycota and Ascomycota, and more rarely from the Zygomycota. Ectomycorrhizas form on the roots of around 2% of plant species, usually woody plants, including species from the birch, dipterocarp, myrtle, beech, willow, pine and rose families. Research on ectomycorrhizas is increasingly important in areas such as ecosystem management and restoration, forestry and agriculture.

Paraburkholderia rhizoxinica is a gram-negative, oxidase and catalase-positiv, motile bacterium from the genus Paraburkholderia and the family Burkholderiaceae which was isolated from the plant pathogenic fungus, Rhizopus microsporus. The complete genome of Paraburkholderia rhizoxinica is sequenced.

Root microbiome

The root microbiome is the dynamic community of microorganisms associated with plant roots. Because they are rich in a variety of carbon compounds, plant roots provide unique environments for a diverse assemblage of soil microorganisms, including bacteria, fungi and archaea. The microbial communities inside the root and in the rhizosphere are distinct from each other, and from the microbial communities of bulk soil, although there is some overlap in species composition.

Mycorrhiza helper bacteria Group of organisms

Mycorrhiza helper bacteria (MHB) are a group of organisms that form symbiotic associations with both ectomycorrhiza and arbuscular mycorrhiza. MHBs are diverse and belong to a wide variety of bacterial phyla including both Gram-negative and Gram-positive bacteria. Some of the most common MHBs observed in studies belong to the phylas Pseudomonas and Streptomyces. MHBs have been seen to have extremely specific interactions with their fungal hosts at times, but this specificity is lost with plants. MHBs enhance mycorrhizal function, growth, nutrient uptake to the fungus and plant, improve soil conductance, aid against certain pathogens, and help promote defense mechanisms. These bacteria are naturally present in the soil, and form these complex interactions with fungi as plant root development starts to take shape. The mechanisms through which these interactions take shape are not well-understood and needs further study.

Hemibiotrophs are the spectrum of plant pathogens, including bacteria, oomycete and a group of plant pathogenic fungi that keep its host alive while establishing itself within the host tissue, taking up the nutrients with brief biotrophic-like phase. It then, in later stages of infection switches to a necrotrophic life-style, where it rampantly kills the host cells, deriving its nutrients from the dead tissues.

Candidatus "Glomeribacter gigasporarum" is a gram-negative β-proteobacteria. The bacterium is rod-shaped, and has a obligate endosymbiotic relationship with the arbuscular-mycorrhizal fungi Gigaspora margarita. Sequencing of the16S rRNA gene places Ca. "G. gigasporarum" within the Burkholderia genus. Ca. "G. gigasporarum is unculturable as of yet, but can stay alive in enrichment for up to 4 weeks. The candidate bacteria is considered "the smallest beta-proteobacterium" with a genome size of 1.4 Mb. The chromosome is 750 kb long and a plasmid is 600 to 650 kb. The genome size was determined using gel-electrophoresis.

References

  1. P. Frey-Klett; P. Burlinson; A. Deveau; M. Barret; M. Tarkka; A. Sarniguet (1 December 2011). "Bacterial-Fungal Interactions: Hyphens between Agricultural, Clinical, Environmental, and Food Microbiologists". Microbiology and Molecular Biology Reviews. 75 (4): 583–609. doi:10.1128/MMBR.00020-11. PMC   3232736 . PMID   22126995.
  2. Manfred Kluge (1 September 2002). "A Fungust eats a Cyanobacterium: The Story of the Geosiphon pyriformis Endocyanosis". Biology and Environment: Proceedings of the Royal Irish Academy. 102B (1): 11–14. JSTOR   20500133.

Further reading