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Endophytic Actinobacteria and the Interaction of Micromonospora and Nitrogen Fixing Plants.

Trujillo ME, Riesco R, Benito P, Carro L - Front Microbiol (2015)

Bottom Line: For a long time, it was believed that a healthy plant did not harbor any microorganisms within its tissues, as these were often considered detrimental for the plant.Micromonospora is a Gram-positive bacterium with a wide geographical distribution; it can be found in the soil, mangrove sediments, and freshwater and marine ecosistems.Unexpectedly, a high number of plant-cell wall degrading enzymes were also detected, a trait usually found only in pathogenic bacteria.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Microbiología y Genética, Universidad de Salamanca Salamanca, Spain.

ABSTRACT
For a long time, it was believed that a healthy plant did not harbor any microorganisms within its tissues, as these were often considered detrimental for the plant. In the last three decades, the numbers of studies on plant microbe-interactions has led to a change in our view and we now know that many of these invisible partners are essential for the overall welfare of the plant. The application of Next Generation Sequencing techniques is a powerful tool that has permitted the detection and identification of microbial communities in healthy plants. Among the new plant microbe interactions recently reported several actinobacteria such as Micromonospora are included. Micromonospora is a Gram-positive bacterium with a wide geographical distribution; it can be found in the soil, mangrove sediments, and freshwater and marine ecosistems. In the last years our group has focused on the isolation of Micromonospora strains from nitrogen fixing nodules of both leguminous and actinorhizal plants and reported for the first time its wide distribution in nitrogen fixing nodules of both types of plants. These studies have shown how this microoganism had been largely overlooked in this niche due to its slow growth. Surprisingly, the genetic diversity of Micromonospora strains isolated from nodules is very high and several new species have been described. The current data indicate that Micromonospora saelicesensis is the most frequently isolated species from the nodular tissues of both leguminous and actinorhizal plants. Further studies have also been carried out to confirm the presence of Micromonospora inside the nodule tissues, mainly by specific in situ hybridization. The information derived from the genome of the model strain, Micromonospora lupini, Lupac 08, has provided useful information as to how this bacterium may relate with its host plant. Several strategies potentially necessary for Micromonospora to thrive in the soil, a highly competitive, and rough environment, and as an endophytic bacterium with the capacity to colonize the internal plant tissues which are protected from the invasion of other soil microbes were identified. The genome data also revealed the potential of M. lupini Lupac 08 as a plant growth promoting bacterium. Several loci involved in plant growth promotion features such as the production of siderophores, phytohormones, and the degradation of chitin (biocontrol) were also located on the genome and the functionality of these genes was confirmed in the laboratory. In addition, when several host plants species were inoculated with Micromonospora strains, the plant growth enhancing effect was evident under greenhouse conditions. Unexpectedly, a high number of plant-cell wall degrading enzymes were also detected, a trait usually found only in pathogenic bacteria. Thus, Micromonospora can be added to the list of new plant-microbe interactions. The current data indicate that this microorganism may have an important application in agriculture and other biotechnological processes. The available information is promising but limited, much research is still needed to determine which is the ecological function of Micromonospora in interaction with nitrogen fixing plants.

No MeSH data available.


Related in: MedlinePlus

Circular genome representation of Micromonospora lupini, Lupac 08. (A) Distribution of various plant-cell wall hydrolytic enzyme loci. Red, cellulases, and cellulose-binding sites; blue, pectinases; yellow, xylanases. (B)In vitro cellulase degradation. (C)In vitro starch degradation. (D)In vitro xylanase degradation (Based on Trujillo et al., 2014b).
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Figure 3: Circular genome representation of Micromonospora lupini, Lupac 08. (A) Distribution of various plant-cell wall hydrolytic enzyme loci. Red, cellulases, and cellulose-binding sites; blue, pectinases; yellow, xylanases. (B)In vitro cellulase degradation. (C)In vitro starch degradation. (D)In vitro xylanase degradation (Based on Trujillo et al., 2014b).

Mentions: The genome of strain Lupac 08 contains a high number of genes encoding enzymes potentially involved in plant cell wall degradation. Approximately 10% of the genome codes for carbohydrate metabolism, and almost 200 out of the 685 genes have a putative hydrolytic function. Hydrolytic activities for cellulose, pectin, starch, and xylan, were confirmed in the laboratory and indicate that this strain could degrade plant cell wall components in a way similar to that of phytopathogen bacteria (Trujillo et al., 2014b). Plant-polymer degrading enzymes are thought to be involved in internal plant colonization (Compant et al., 2005). Plant pathogenic fungi and bacteria usually enter plant tissues by degrading plant cell wall components using several hydrolases which include cellulases and endoglucanases. On the other hand, genome data show that non-pathogenic (endophytic or symbiotic) microorganisms contain a low set of plant-polymer degrading enzymes (Krause et al., 2007; Mastronunzio et al., 2008; Taghavi et al., 2010). In the case of M lupini, the genome of this microorganism revealed a high number of hydrolytic enzymes (e.g., cellulases, xylanases, endoglucanases) with the potential to degrade plant tissues (Figure 3). However, green-house experiments show that when host plants are inoculated with strain Lupac 08 no damage is produced. On the contrary, M. lupini stimulates nodulation and plant growth (Cerda, 2008; Trujillo et al., 2014b). Therefore, if the plant does appear to be negatively affected by these enzymes, what is their potential function when the bacterium interacts with its host plant? Our group is currently working on this subject, some of the loci, especially those related to cellulose metabolism may participate in other processes such as cellulose biosynthesis (Robledo et al., 2008, 2012; Mba Medie et al., 2012). Several genes coding for plant cell-wall degrading enzymes were also located in the genome of Micromonospora sp. L5 (Hirsch et al., 2013). Similarly to strain Lupac 08, target substrates include cellulose, hemicellulose, pectin, starch, and xylan, however, the number of loci involved in carbohydrate transport and metabolism are slightly lower in strain L5 (8.9%), as compared to strain Lupac 08 (9.7%) (Trujillo et al., 2014b).


Endophytic Actinobacteria and the Interaction of Micromonospora and Nitrogen Fixing Plants.

Trujillo ME, Riesco R, Benito P, Carro L - Front Microbiol (2015)

Circular genome representation of Micromonospora lupini, Lupac 08. (A) Distribution of various plant-cell wall hydrolytic enzyme loci. Red, cellulases, and cellulose-binding sites; blue, pectinases; yellow, xylanases. (B)In vitro cellulase degradation. (C)In vitro starch degradation. (D)In vitro xylanase degradation (Based on Trujillo et al., 2014b).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4664631&req=5

Figure 3: Circular genome representation of Micromonospora lupini, Lupac 08. (A) Distribution of various plant-cell wall hydrolytic enzyme loci. Red, cellulases, and cellulose-binding sites; blue, pectinases; yellow, xylanases. (B)In vitro cellulase degradation. (C)In vitro starch degradation. (D)In vitro xylanase degradation (Based on Trujillo et al., 2014b).
Mentions: The genome of strain Lupac 08 contains a high number of genes encoding enzymes potentially involved in plant cell wall degradation. Approximately 10% of the genome codes for carbohydrate metabolism, and almost 200 out of the 685 genes have a putative hydrolytic function. Hydrolytic activities for cellulose, pectin, starch, and xylan, were confirmed in the laboratory and indicate that this strain could degrade plant cell wall components in a way similar to that of phytopathogen bacteria (Trujillo et al., 2014b). Plant-polymer degrading enzymes are thought to be involved in internal plant colonization (Compant et al., 2005). Plant pathogenic fungi and bacteria usually enter plant tissues by degrading plant cell wall components using several hydrolases which include cellulases and endoglucanases. On the other hand, genome data show that non-pathogenic (endophytic or symbiotic) microorganisms contain a low set of plant-polymer degrading enzymes (Krause et al., 2007; Mastronunzio et al., 2008; Taghavi et al., 2010). In the case of M lupini, the genome of this microorganism revealed a high number of hydrolytic enzymes (e.g., cellulases, xylanases, endoglucanases) with the potential to degrade plant tissues (Figure 3). However, green-house experiments show that when host plants are inoculated with strain Lupac 08 no damage is produced. On the contrary, M. lupini stimulates nodulation and plant growth (Cerda, 2008; Trujillo et al., 2014b). Therefore, if the plant does appear to be negatively affected by these enzymes, what is their potential function when the bacterium interacts with its host plant? Our group is currently working on this subject, some of the loci, especially those related to cellulose metabolism may participate in other processes such as cellulose biosynthesis (Robledo et al., 2008, 2012; Mba Medie et al., 2012). Several genes coding for plant cell-wall degrading enzymes were also located in the genome of Micromonospora sp. L5 (Hirsch et al., 2013). Similarly to strain Lupac 08, target substrates include cellulose, hemicellulose, pectin, starch, and xylan, however, the number of loci involved in carbohydrate transport and metabolism are slightly lower in strain L5 (8.9%), as compared to strain Lupac 08 (9.7%) (Trujillo et al., 2014b).

Bottom Line: For a long time, it was believed that a healthy plant did not harbor any microorganisms within its tissues, as these were often considered detrimental for the plant.Micromonospora is a Gram-positive bacterium with a wide geographical distribution; it can be found in the soil, mangrove sediments, and freshwater and marine ecosistems.Unexpectedly, a high number of plant-cell wall degrading enzymes were also detected, a trait usually found only in pathogenic bacteria.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Microbiología y Genética, Universidad de Salamanca Salamanca, Spain.

ABSTRACT
For a long time, it was believed that a healthy plant did not harbor any microorganisms within its tissues, as these were often considered detrimental for the plant. In the last three decades, the numbers of studies on plant microbe-interactions has led to a change in our view and we now know that many of these invisible partners are essential for the overall welfare of the plant. The application of Next Generation Sequencing techniques is a powerful tool that has permitted the detection and identification of microbial communities in healthy plants. Among the new plant microbe interactions recently reported several actinobacteria such as Micromonospora are included. Micromonospora is a Gram-positive bacterium with a wide geographical distribution; it can be found in the soil, mangrove sediments, and freshwater and marine ecosistems. In the last years our group has focused on the isolation of Micromonospora strains from nitrogen fixing nodules of both leguminous and actinorhizal plants and reported for the first time its wide distribution in nitrogen fixing nodules of both types of plants. These studies have shown how this microoganism had been largely overlooked in this niche due to its slow growth. Surprisingly, the genetic diversity of Micromonospora strains isolated from nodules is very high and several new species have been described. The current data indicate that Micromonospora saelicesensis is the most frequently isolated species from the nodular tissues of both leguminous and actinorhizal plants. Further studies have also been carried out to confirm the presence of Micromonospora inside the nodule tissues, mainly by specific in situ hybridization. The information derived from the genome of the model strain, Micromonospora lupini, Lupac 08, has provided useful information as to how this bacterium may relate with its host plant. Several strategies potentially necessary for Micromonospora to thrive in the soil, a highly competitive, and rough environment, and as an endophytic bacterium with the capacity to colonize the internal plant tissues which are protected from the invasion of other soil microbes were identified. The genome data also revealed the potential of M. lupini Lupac 08 as a plant growth promoting bacterium. Several loci involved in plant growth promotion features such as the production of siderophores, phytohormones, and the degradation of chitin (biocontrol) were also located on the genome and the functionality of these genes was confirmed in the laboratory. In addition, when several host plants species were inoculated with Micromonospora strains, the plant growth enhancing effect was evident under greenhouse conditions. Unexpectedly, a high number of plant-cell wall degrading enzymes were also detected, a trait usually found only in pathogenic bacteria. Thus, Micromonospora can be added to the list of new plant-microbe interactions. The current data indicate that this microorganism may have an important application in agriculture and other biotechnological processes. The available information is promising but limited, much research is still needed to determine which is the ecological function of Micromonospora in interaction with nitrogen fixing plants.

No MeSH data available.


Related in: MedlinePlus