Global analyses of biosynthetic gene clusters in phytobiomes reveal strong phylogenetic conservation of terpenes and aryl polyenes
ABSTRACT There are gaps in our understandings on how did the evolutionary relationships among members of the phytobiomes shape their ability to produce tremendously complex specialized metabolites under the influence of plant host. To determine these relationships, we investigated the phylogenetic c...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-08-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00387-23 |
| _version_ | 1797730338849423360 |
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| author | Arijit Mukherjee Hitesh Tikariha Aditya Bandla Shruti Pavagadhi Sanjay Swarup |
| author_facet | Arijit Mukherjee Hitesh Tikariha Aditya Bandla Shruti Pavagadhi Sanjay Swarup |
| author_sort | Arijit Mukherjee |
| collection | DOAJ |
| description | ABSTRACT There are gaps in our understandings on how did the evolutionary relationships among members of the phytobiomes shape their ability to produce tremendously complex specialized metabolites under the influence of plant host. To determine these relationships, we investigated the phylogenetic conservation of biosynthetic gene clusters (BGCs) on a global collection of 4,519 high-quality and nonredundant (out of 12,181) bacterial isolates and metagenome-assembled genomes from 47 different plant hosts and soil, by adopting three independent phylogenomic approaches (D-test, Pagel’s λ, and consenTRAIT). We report that the BGCs are phylogenetically conserved to varying strengths and depths in their different classes. We show that the ability to produce specialized metabolites qualifies as a complex trait, and the depth of conservation is equivalent to ecologically relevant complex microbial traits. Interestingly, terpene and aryl polyene BGCs had the strongest phylogenetic conservation in the phytobiomes, but not in the soil microbiomes. Furthermore, we showed that terpenes are largely uncharacterized in phytobiomes and pinpointed specific clades that harbor potentially novel terpenes. Taken together, this study sheds light on the evolution of specialized metabolites’ biosynthesis potential in phytobiomes under the influence of plant hosts and presents strategies to rationally guide the discovery of potentially novel classes of metabolites. IMPORTANCE This study expands our understandings of the biosynthetic potential of phytobiomes by using such worldwide and extensive collection of microbiomes from plants and soil. Apart from providing such vital resource for the plant microbiome researchers, this study provides fundamental insights into the evolution of biosynthetic gene clusters (BGCs) in phytobiomes under the influence of plant host. Specifically, we report that the strength of phylogenetic conservation in microbiomes varies for different classes of BGCs and is influenced as a result of plant host association. Furthermore, our results indicate that biosynthetic potential of specialized metabolites is deeply conserved equivalent to other complex and ecologically relevant microbial traits. Finally, for the most conserved class of specialized metabolites (terpenes), we identified clades harboring potentially novel class of molecules. Future studies could focus on plant–microbe coevolution and interactions through specialized metabolites building upon these findings. |
| first_indexed | 2024-03-12T11:42:51Z |
| format | Article |
| id | doaj.art-b432389f94454b20869c8acbcf8cce6d |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-03-12T11:42:51Z |
| publishDate | 2023-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-b432389f94454b20869c8acbcf8cce6d2023-08-31T13:00:43ZengAmerican Society for MicrobiologymSystems2379-50772023-08-018410.1128/msystems.00387-23Global analyses of biosynthetic gene clusters in phytobiomes reveal strong phylogenetic conservation of terpenes and aryl polyenesArijit Mukherjee0Hitesh Tikariha1Aditya Bandla2Shruti Pavagadhi3Sanjay Swarup4Department of Biological Sciences, National University of Singapore , Singapore, SingaporeDepartment of Biological Sciences, National University of Singapore , Singapore, SingaporeSingapore Centre for Environmental Life Sciences Engineering, National University of Singapore , Singapore, SingaporeSingapore Centre for Environmental Life Sciences Engineering, National University of Singapore , Singapore, SingaporeDepartment of Biological Sciences, National University of Singapore , Singapore, SingaporeABSTRACT There are gaps in our understandings on how did the evolutionary relationships among members of the phytobiomes shape their ability to produce tremendously complex specialized metabolites under the influence of plant host. To determine these relationships, we investigated the phylogenetic conservation of biosynthetic gene clusters (BGCs) on a global collection of 4,519 high-quality and nonredundant (out of 12,181) bacterial isolates and metagenome-assembled genomes from 47 different plant hosts and soil, by adopting three independent phylogenomic approaches (D-test, Pagel’s λ, and consenTRAIT). We report that the BGCs are phylogenetically conserved to varying strengths and depths in their different classes. We show that the ability to produce specialized metabolites qualifies as a complex trait, and the depth of conservation is equivalent to ecologically relevant complex microbial traits. Interestingly, terpene and aryl polyene BGCs had the strongest phylogenetic conservation in the phytobiomes, but not in the soil microbiomes. Furthermore, we showed that terpenes are largely uncharacterized in phytobiomes and pinpointed specific clades that harbor potentially novel terpenes. Taken together, this study sheds light on the evolution of specialized metabolites’ biosynthesis potential in phytobiomes under the influence of plant hosts and presents strategies to rationally guide the discovery of potentially novel classes of metabolites. IMPORTANCE This study expands our understandings of the biosynthetic potential of phytobiomes by using such worldwide and extensive collection of microbiomes from plants and soil. Apart from providing such vital resource for the plant microbiome researchers, this study provides fundamental insights into the evolution of biosynthetic gene clusters (BGCs) in phytobiomes under the influence of plant host. Specifically, we report that the strength of phylogenetic conservation in microbiomes varies for different classes of BGCs and is influenced as a result of plant host association. Furthermore, our results indicate that biosynthetic potential of specialized metabolites is deeply conserved equivalent to other complex and ecologically relevant microbial traits. Finally, for the most conserved class of specialized metabolites (terpenes), we identified clades harboring potentially novel class of molecules. Future studies could focus on plant–microbe coevolution and interactions through specialized metabolites building upon these findings.https://journals.asm.org/doi/10.1128/msystems.00387-23biosynthetic gene clustersphylogenetic conservationplant microbiomesqualene hopene cyclasesqualene phytoene synthaseterpenes |
| spellingShingle | Arijit Mukherjee Hitesh Tikariha Aditya Bandla Shruti Pavagadhi Sanjay Swarup Global analyses of biosynthetic gene clusters in phytobiomes reveal strong phylogenetic conservation of terpenes and aryl polyenes mSystems biosynthetic gene clusters phylogenetic conservation plant microbiome squalene hopene cyclase squalene phytoene synthase terpenes |
| title | Global analyses of biosynthetic gene clusters in phytobiomes reveal strong phylogenetic conservation of terpenes and aryl polyenes |
| title_full | Global analyses of biosynthetic gene clusters in phytobiomes reveal strong phylogenetic conservation of terpenes and aryl polyenes |
| title_fullStr | Global analyses of biosynthetic gene clusters in phytobiomes reveal strong phylogenetic conservation of terpenes and aryl polyenes |
| title_full_unstemmed | Global analyses of biosynthetic gene clusters in phytobiomes reveal strong phylogenetic conservation of terpenes and aryl polyenes |
| title_short | Global analyses of biosynthetic gene clusters in phytobiomes reveal strong phylogenetic conservation of terpenes and aryl polyenes |
| title_sort | global analyses of biosynthetic gene clusters in phytobiomes reveal strong phylogenetic conservation of terpenes and aryl polyenes |
| topic | biosynthetic gene clusters phylogenetic conservation plant microbiome squalene hopene cyclase squalene phytoene synthase terpenes |
| url | https://journals.asm.org/doi/10.1128/msystems.00387-23 |
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