It has been shown that these bladders fix CO 2 , which may be the major contribution of the cyanobacterium to the symbiosis. The symbiont also forms heterocysts, suggesting that nitrogen is fixed as well [ 56 ]. However, as these heterocysts are somewhat similar to those of free-living relatives of this Nostoc strain, nitrogen fixation may only serve the needs of the symbiont itself. Interactions of bacteria with various groups of plants are the most common symbiotic association for nitrogen assimilation.
A multiplicity of bacteria with different physiological backgrounds are involved in these associations, including gram-negative proteobacteria like Rhizobia sp.
The physiological and morphological characteristics of these symbioses range from extracellular communities to highly adapted interfaces within special organs or compartments. The mutualistic symbioses between various non-photosynthetic proteobacteria of the order Rhizobiales with plants of the orders Fabales, Fagales, Curcurbitales and Rosales are the most extensively studied interactions between bacteria and plants [ 59 ].
The rhizobia-legume symbiosis is characterised by typical root-nodule structures of the plant host, which are colonised by the endosymbiotic rhizobia, so-called bacteroids [ 60 ]. The nodulated plant roots supply the bacteria with energy-rich carbon compounds and obtain fixed nitrogen by the bacteroids in return. The nodule formation is a highly regulated and complex process driven by both partners.
Free-living rhizobia enter the plant root epidermis and induce nodule formation by reprogramming root cortical cells.
Of special importance for the establishment of the symbiosis are flavonoids secreted by the plant partner [ 61 ] and the subsequent induction of bacterial nodulation nod genes [ 62 ]. The Nod-factors play a role in the formation of the nodule, a complex structure optimised for the requirements of both partners [ 63 , 64 ]. Analysis of root epidermal infection and the underlying signal transduction pathways [ 65 — 67 ] indicate that Nod-factors may have evolved following recruitment of pathways, which developed in a phylogenetically more ancient arbuscular mycorrhiza symbiosis [ 68 , 69 ].
In the nodule, bacteroids reside within parenchym cells, where they are localised in membrane bound vesicles Figure 3a [ 70 ]. Nitrogenase activity is ensured by the spatial separation of the bacteroids inside the nodule structure and special oxygen-scavenging leghemoglobin that is synthesised in the nodules [ 71 ]. An interesting feature of rhizobia is that nitrogen fixation is restricted to symbiotic bacteroids, whereas free-living bacteria do not express nitrogenase [ 72 ]. Although the rhizobia-legume symbiosis is a highly adapted and regulated interaction it can not be termed permanent or obligate.
Both partners can live and propagate autonomously, and each host generation has to be populated by a new strain of free-living rhizobia. Rhizobia-legume symbioses are not the only root-nodule forming interactions of bacteria and plants. Actinobacteria of the genus Frankia spp. Free-living Frankia is characterised by a unique morphology, including three structural forms, hypha, sporangium and vesicle, the latter one being a compartment for nitrogen fixation.
Although functionally analogous, Frankia nodules differ from those in rhizobia-legume interactions in development and morphology [ 74 ].
In contrast to rhizobia all Frankia strains are also capable of fixing molecular nitrogen as free-living bacteria [ 75 ]. The appearance of the Frankia -symbiosis as a nodulation dependent interaction emphasises the adaptation of both partners. Other plants, including important economic crops like Zea mays and Oryza sativa have established associations with different nitrogen-fixing bacteria, including Azospirillum [ 76 ] and Azoarcus [ 77 ].
However, such symbioses have never been found to result in nodule formation. Endosymbionts adapted for molecular nitrogen fixation a A Bradyrhizobium sp. In addition, nitrogen fixing cyanobacteria are also often found interacting with plant partners. For example, symbioses of filamentous heterocyst-forming Nostoc sp.
In all plant hosts, with the exception of Gunnera , symbiotic Nostoc filaments are localised extracellularly in different locations depending on the host species. In bryophytes, like hornworts, the cyanobacteria are found within cavities of the gametophyte [ 79 ], whereas an Azolla sp. In cycad-cyanobacterial associations the symbionts are limited to specialised coralloid roots where they reside in the cortical cyanobacterial zone [ 81 ]. More specialised is the mutualistic intracellular Gunnera - Nostoc symbiosis. Here the process begins with invasion of the petiole glands, followed by intracellular establishment within the meristematic cells of this tissue [ 60 , 78 ].
The symbioses of cyanobacteria with their plant partners differ remarkably from the rhizobia-legume interactions.
First, cyanobacteria show a broad host range and thus differ from rhizobia or Frankia sp. In addition, cyanobacteria do not induce the formation of highly specialised structures like root-nodules after colonisation of the host but reside in plant structures known as symbiotic cavities [ 82 ], which also exist without symbiosis. The lack of nodule-like organs can be explained by the fact that heterocyst forming cyanobacteria also fix nitrogen as free-living cells and therefore do not need a special environment for N 2 -fixation in symbiosis.
This makes them distinct from rhizobia, which only fix nitrogen in the protective environment of the nodule.
Although symbiotic cavities do not display the close and highly regulated interface of a legume-nodule they are nevertheless regions that exhibit adaptations for symbiosis. A common specialisation in occupied symbiotic cavities of plant hosts is the elaboration of elongated cells to improve nutrient exchange [ 83 ] and the production of mucilage-exopolysaccharides for water storage or as nutrient reserve e. The infection process is controlled via the production of hormogenium-inducing factors by the host plant, resulting in the development of vegetative cyanobacterial filaments hormogonia , important for host colonisation [ 86 , 87 ].
The main adaptations to the symbiotic lifestyle found in the bacterial partners concern changes of morphology and physiology. These include a remarkable increase of heterocysts in symbiotic Nostoc , and higher rates of N 2 fixation compared to those of free-living cells. In addition, photosynthesis of symbiotic cyanobacteria is depressed in various associations to avoid competition between symbionts and host for CO 2 and light [ 86 ]. In conclusion, different adaptations are found in cyanobacterial-plant interactions but they are not as specific and highly regulated as the complex nodule-forming symbioses.
A common feature of all bacteria plant symbioses is their non-obligate, non-permanent character, including a lack of vertical transmission of symbionts to the next host generation. An exception might be the Nostoc - Azolla symbiosis, where cyanobacterial homogenia are transmitted via megaspores [ 88 ].
Symbioses of bacteria with unicellular eukaryotes are exceptional as they involve the whole host rather than specialised parts of the host organism. Also these intracellular symbionts require a high degree of regulation and adaptation to maintain the mutualistic relationship. This feature, in conjunction with vertical transmission, suggests that co-evolution and dependence of partners is sufficiently advanced to regard the relationship as unification of two single organisms.
The mitochondria and plastids of recent eukaryotes are extreme examples of this kind of association [ 89 , 90 ]. Cyanobacteria have also been detected in intracellular association with an euglenoid flagellate [ 91 ], heterotrophic dinoflagellates [ 92 — 94 ], a filose amoeba [ 95 ], diatoms [ 96 , 97 ] and, extracellularly, with some protists, e. Only rarely has the nitrogen fixing activity of the prokaryotic partner been demonstrated in these symbioses e.
In the next paragraph the range of symbiotic associations between cyanobacteria and protists is described in a progression of interactions from temporary to permanent. As such, these symbioses provide an opportunity to investigate the cellular changes that may accompany the evolutionary transition from extracellular symbiont to intracellular endosymbiont and cell organelle.
Editors: Rai, A.N., Bergman, B., Rasmussen, Ulla (Eds.) Cyanobacterial symbioses are no longer regarded as mere oddities but as important components of the biosphere, occurring both in terrestrial and aquatic habitats worldwide. It is becoming apparent that they can enter into. Cycads establish symbioses with filamentous cyanobacteria in highly specialised lateral roots termed “coralloid roots”. The coralloid roots.
Petalomonas sphagnophila is an apoplastic euglenoid that harbours endosymbiotic Synechocystis species [ 91 ]. The cyanobacteria occur inside a perialgal vacuole and remain alive for several weeks, before they are metabolised, so that they must be regarded as temporary endosymbiotic cell inclusions. These intracellular cyanobacteria are thus reminiscent of kleptochloroplasts found in some heterotrophic dinoflagellates, marine snails, foraminifera and ciliates.
These associations can be understood as a mechanism for the temporary separation of ingested and digested prey [ 92 — 94 , ]. However, in all well-documented cases of kleptochloroplastic interactions, only the plastid or the plastid together with surrounding cell compartments never the whole cell is incorporated as a kleptochloroplast by the host. In contrast, the cyanobacteria of P. Symbiont integrity is therefore likely to be a prerequisite for the functioning of the cyanobacterial nitrogen fixing machinery.
The enslaved cyanobacteria may also provide energy-rich C-compounds or, as suggested for other symbiotic interactions, vitamin B12 production to it host [ ]. These hypotheses are yet to be investigated thoroughly.
Phaeosomes are symbionts found in some representatives of the order Dinophysiales. They exhibit morphological characteristics of Synechocystsis and Synechococcus cells and are located either extracellularly or intracellularly [ 94 ]. In the case of intracellular cells, the symbioses seem to be permanent and the benefit of the symbiosis to the host may be efficient nitrogen fixation.
However, as in the case of P. Some filamentous cyanobacteria are known to interact with diatoms. Extracellular epibionts, endosymbionts and also symbionts positioned in the periplasmic space between the cell wall and cell membrane of the diatom are known to occur [ 58 , 98 ]. Electron microscopy scanning of such interactions has demonstrated a dual symbiotic nature of some symbionts.
Richelia intracellularis has been observed to interact either as an epibiont with Chaetoceros spec. In these examples, nitrogen fixation for the benefit of the host has been demonstrated by the cultivation of the symbiont-diatom association in the absence of an external fixed nitrogen source. Nitrogen fixation is also suggested from morphological features such as the presence of heterocysts.
At least in tropical environments, the production of B12 vitamins may also be a further benefit for the host [ ]. Some diatoms, including Climacodium frauenfeldianum and Rhopalodia gibba , are known to harbour permanent endosymbionts [ 96 , 97 , ]. As indicated by EM investigations of R.
The endosymbionts, so-called spheroid bodies [ 96 ], are localised in the cytoplasm, and separated by a perialgal vacuole from the cytosol. Each spheroid body is surrounded by a double membrane. As additionally internal membranes are also visible, this morphotype is similar to that of cyanobacteria Figure 3b.