A New Perspective of Pseudomonas—Host Interactions: Distribution and Potential Ecological Functions of the Genus Pseudomonas within the Bark Beetle Holobiont

Saati‐Santamaría, Zaki; Rivas, Raúl; Kolařík, Miroslav; García‐Fraile, Paula

doi:10.3390/biology10020164

Cited by 32 publications

(23 citation statements)

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“… Pseudomonas is one of the most diverse and ubiquitous bacterial genera in nature. It is commonly found associated with animals, plants, soil, water and many other ecological niches, where these organisms can endure highly diverse environmental conditions [17–20]. To survive and compete in these micro-habitats, Pseudomonas strains can produce a repertoire of secondary metabolites, which protect them from extreme conditions or aid in the fight against other microbial competitors in the same niche [17, 21, 22].…”

Section: Introductionmentioning

confidence: 99%

Unveiling the genomic potential of Pseudomonas type strains for discovering new natural products

Saati‐Santamaría

Sélem-Mójica²,

Peral-Aranega

et al. 2022

Microbial Genomics

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Microbes host a huge variety of biosynthetic gene clusters that produce an immeasurable array of secondary metabolites with many different biological activities such as antimicrobial, anticarcinogenic and antiviral. Despite the complex task of isolating and characterizing novel natural products, microbial genomic strategies can be useful for carrying out these types of studies. However, although genomic-based research on secondary metabolism is on the increase, there is still a lack of reports focusing specifically on the genus Pseudomonas . In this work, we aimed (i) to unveil the main biosynthetic systems related to secondary metabolism in Pseudomonas type strains, (ii) to study the evolutionary processes that drive the diversification of their coding regions and (iii) to select Pseudomonas strains showing promising results in the search for useful natural products. We performed a comparative genomic study on 194 Pseudomonas species, paying special attention to the evolution and distribution of different classes of biosynthetic gene clusters and the coding features of antimicrobial peptides. Using EvoMining, a bioinformatic approach for studying evolutionary processes related to secondary metabolism, we sought to decipher the protein expansion of enzymes related to the lipid metabolism, which may have evolved toward the biosynthesis of novel secondary metabolites in Pseudomonas . The types of metabolites encoded in Pseudomonas type strains were predominantly non-ribosomal peptide synthetases, bacteriocins, N-acetylglutaminylglutamine amides and ß-lactones. Also, the evolution of genes related to secondary metabolites was found to coincide with Pseudomonas species diversification. Interestingly, only a few Pseudomonas species encode polyketide synthases, which are related to the lipid metabolism broadly distributed among bacteria. Thus, our EvoMining-based search may help to discover new types of secondary metabolite gene clusters in which lipid-related enzymes are involved. This work provides information about uncharacterized metabolites produced by Pseudomonas type strains, whose gene clusters have evolved in a species-specific way. Our results provide novel insight into the secondary metabolism of Pseudomonas and will serve as a basis for the prioritization of the isolated strains. This article contains data hosted by Microreact.

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Section: Introductionmentioning

confidence: 99%

Unveiling the genomic potential of Pseudomonas type strains for discovering new natural products

Saati‐Santamaría

Sélem-Mójica²,

Peral-Aranega

et al. 2022

Microbial Genomics

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“…For example, Serratia and Acinetobacter can increase host resistance to insecticides, 48,49,64 Pantoea-lacking Halyomorpha halys exhibit developmental delays and abnormal behaviors 65 and Pseudomonas can provide essential nutrients for bark beetles and protect their host from phytochemical defenses of pathogenic fungi. 66 The bacterial functions only differed between NLS and NLW in nymphs, which may be related to the different relative abundances of the two Wolbachia strains. Except nymphs, most of the differing bacterial functions between NLW/NLUI and NLS/NLUI were identical, which indicates a similar effect of the two Wolbachia strains on bacterial functions.…”

Section: Discussionmentioning

confidence: 97%

“…Many bacteria play important roles in the physiological functions of their insect hosts. For example, Serratia and Acinetobacter can increase host resistance to insecticides, 48,49,64 Pantoea ‐lacking Halyomorpha halys exhibit developmental delays and abnormal behaviors 65 and Pseudomonas can provide essential nutrients for bark beetles and protect their host from phytochemical defenses of pathogenic fungi 66 . The bacterial functions only differed between NLS and NLW in nymphs, which may be related to the different relative abundances of the two Wolbachia strains.…”

Section: Discussionmentioning

confidence: 99%

Recently introducedWolbachiareduces bacterial species richness and reshapes bacterial community structure inNilaparvata lugens

Zhou

Gong

et al. 2022

Pest Management Science

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BACKGROUND Wolbachia has been developed as an effective tool to suppress insect pests and arbovirus transmission. Recently, the brown planthopper Nilaparvata lugens, a serious agricultural pest, has been successfully transinfected with Wolbachia wStri strain from Laodelphax striatellus. However, before conducting the field experiments, the impacts of wStri on the bacterial microbiota in N. lugens and how it differs from native Wolbachia wLug strain have not been clarified. RESULTS Here, we found that wStri reduced bacterial diversity and shaped bacterial community structure more than wLug in both developmental stage and different adult tissues. Overall, the relative abundance of Wolbachia was negatively correlated with bacterial diversity, but the bacterial diversity gradually decreased only when the relative abundance of Wolbachia was higher than 60%. Further analysis found that wStri reduced species richness of other bacteria but not their evenness. wStri infection also affected many bacterial functions (e.g., amino acid metabolism & signaling and cellular processes) in the developmental stages, with a stronger effect than wLug in nymphs. Moreover, although Wolbachia occupied a high relative abundance in infected individuals, Acinetobacter was consistently a core part of microbiome. CONCLUSION These results showed the significant impacts of recently introduced wStri on bacterial microbiota in N. lugens, with the effects differing from native wLug. This study will aid in understanding the relationship between Wolbachia, its host and the host’s microbiota, and provide a reference for future field experiments.

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“…Also, a naringenin-degrading bacterial community associated with Dendroctonus valens externally detoxify such phenolic compound ( Cheng et al, 2018 ). Bacterial species associated with the bark beetles symbioses tolerate and metabolize terpenes and phenolic compounds, inhibit antagonistic fungi, possibly provide carbon and nitrogen to the host beetle, and encode pathways for degrading lignocellulose ( Morales-Jiménez et al, 2009 , 2012 , 2013 ; Menéndez et al, 2015 ; Fabryová et al, 2018 ; García-Fraile, 2018 ; Xu et al, 2019 ; Peral-Aranega et al, 2020 ; Saati-Santamaría et al, 2021 ). Pseudomonas spp., in particular, have been consistently found in diverse bark beetle species, in diverse niches, and throughout the beetle lifecycle, hypothesized as a consistent member of the beetle-fungal symbiosis ( Saati-Santamaría et al, 2021 ).…”

Section: Plant-degrading Microbial Communities From Insect Fungiculturementioning

confidence: 99%

Lessons From Insect Fungiculture: From Microbial Ecology to Plastics Degradation

Barcoto

Rodrigues

2022

Front. Microbiol.

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Anthropogenic activities have extensively transformed the biosphere by extracting and disposing of resources, crossing boundaries of planetary threat while causing a global crisis of waste overload. Despite fundamental differences regarding structure and recalcitrance, lignocellulose and plastic polymers share physical-chemical properties to some extent, that include carbon skeletons with similar chemical bonds, hydrophobic properties, amorphous and crystalline regions. Microbial strategies for metabolizing recalcitrant polymers have been selected and optimized through evolution, thus understanding natural processes for lignocellulose modification could aid the challenge of dealing with the recalcitrant human-made polymers spread worldwide. We propose to look for inspiration in the charismatic fungal-growing insects to understand multipartite degradation of plant polymers. Independently evolved in diverse insect lineages, fungiculture embraces passive or active fungal cultivation for food, protection, and structural purposes. We consider there is much to learn from these symbioses, in special from the community-level degradation of recalcitrant biomass and defensive metabolites. Microbial plant-degrading systems at the core of insect fungicultures could be promising candidates for degrading synthetic plastics. Here, we first compare the degradation of lignocellulose and plastic polymers, with emphasis in the overlapping microbial players and enzymatic activities between these processes. Second, we review the literature on diverse insect fungiculture systems, focusing on features that, while supporting insects’ ecology and evolution, could also be applied in biotechnological processes. Third, taking lessons from these microbial communities, we suggest multidisciplinary strategies to identify microbial degraders, degrading enzymes and pathways, as well as microbial interactions and interdependencies. Spanning from multiomics to spectroscopy, microscopy, stable isotopes probing, enrichment microcosmos, and synthetic communities, these strategies would allow for a systemic understanding of the fungiculture ecology, driving to application possibilities. Detailing how the metabolic landscape is entangled to achieve ecological success could inspire sustainable efforts for mitigating the current environmental crisis.

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A New Perspective of Pseudomonas—Host Interactions: Distribution and Potential Ecological Functions of the Genus Pseudomonas within the Bark Beetle Holobiont

Cited by 32 publications

References 86 publications

Unveiling the genomic potential of Pseudomonas type strains for discovering new natural products

Unveiling the genomic potential of Pseudomonas type strains for discovering new natural products

Recently introducedWolbachiareduces bacterial species richness and reshapes bacterial community structure inNilaparvata lugens

Lessons From Insect Fungiculture: From Microbial Ecology to Plastics Degradation

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