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. 2024 Oct 15:15:1445713.
doi: 10.3389/fpls.2024.1445713. eCollection 2024.

The microbiome and metatranscriptome of a panel from the Sarracenia mapping population reveal complex assembly and function involving host influence

Jiazhang Cai  1 , Iqra Mohsin  2 , Willie Rogers  3 , Mengrui Zhang  4 , Lin Jiang  5 , Russell Malmberg  3 , Magdy Alabady  3
Affiliations

The microbiome and metatranscriptome of a panel from the Sarracenia mapping population reveal complex assembly and function involving host influence

Jiazhang Cai et al. Front Plant Sci. .

Abstract

Sarracenia provide an optimal system for deciphering the host-microbiome interactions at various levels. We analyzed the pitcher microbiomes and metatranscriptomes of the parental species, and F1 and F2 generations from the mapping population (Sarracenia purpurea X Sarracenia psittacina) utilizing high-throughput sequencing methods. This study aimed to examine the host influences on the microbiome structure and function and to identify the key microbiome traits. Our quality datasets included 8,892,553 full-length bacterial 16s rRNA gene sequences and 65,578 assembled metatranscripts with microbial protein annotations. The correlation network of the bacterial microbiome revealed the presence of 3-7 distinct community clusters, with 8 hub and 19 connector genera. The entire microbiome consisted of viruses, bacterial, archaea, and fungi. The richness and diversity of the microbiome varied among the parental species and offspring genotypes despite being under the same greenhouse environmental conditions. We have discovered certain microbial taxa that are genotype-enriched, including the community hub and connector genera. Nevertheless, there were no significant differences observed in the functional enrichment analysis of the metatranscriptomes across the different genotypes, suggesting a functional convergence of the microbiome. We found that the pitcher microcosm harbors both rhizosphere and phyllosphere microbiomes within its boundaries, resulting in a structurally diverse and functionally complex microbiome community. A total of 50,424 microbial metatranscripts were linked to plant growth-promoting microbial proteins. We show that this complex pitcher microbiome possesses various functions that contribute to plant growth promotion, such as biofertilization, bioremediation, phytohormone signaling, stress regulation, and immune response stimulation. Additionally, the pitcher microbiome exhibits traits related to microbe-microbe interactions, such as colonization of plant systems, biofilm formation, and microbial competitive exclusion. In summary, the demonstrated taxonomical divergence and functionally convergence of the pitcher microbiome are impacted by the host genetics, making it an excellent system for discovering novel beneficial microbiome traits.

Keywords: carnivorous plants; metatranscriptome; microbiome; pitcher plant; plant-microbiome interaction; sarracenia; structural and functional core microbiome.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Summary of the experiment and analysis pipelines. (A) Photos of the parents (Spu and Sps) and selected F1 and F2 individuals of the Spu X Sps mapping population, and a sample of the collected pitcher fluid. (B) The experimental process of preparing the pitcher fluid samples and sequencing. (C) Modules of the 16S rRNA microbiome analysis pipeline. (D) Modules of the metatranscriptome RNA analysis pipeline.
Figure 2
Figure 2
Microbiome diversity assessment. (A) Comparison of alpha diversity of different genotypes using Chao, Pielou, and Shannon tests to assess richness, evenness, and both, respectively. (B) Visualization of the relationship between every sample using Principal Coordinate Analysis. The color represents the genotype of each sample. The ellipses mark the variation of each genotype.
Figure 3
Figure 3
The core and genotype enriched microbiome analysis. (A) A Venn diagram showing the number of overlapped genera among Spu, Sps, F1, and F2. (B) Heatmap of the prevalence of different microbiomes under different detection thresholds. The detection value and prevalence cut-off limits are represented by the horizontal red line and transparent area, respectively. (C) Four Venn diagrams comparing the overlapping genera among every three genotypes to highlight the genotype specific numbers. (D) Genotype-enriched genes detected by Linear discriminant analysis Effect Size.
Figure 4
Figure 4
Network analysis. (A) the whole network of 582 filtered genera (left) and connectivity scores (Right). (B-E left) the subnetworks of top 100 genera ranked by their hubscore (B), z-score (C), normalized abundance (D), and participant coefficient (E). The connectivity scores of the four subnetworks are in their corresponding right panels.
Figure 5
Figure 5
Genera overlapping among subnetworks and abundance of hub genera. (A-C) Venn diagrams showing the number of overlapped nodes (genera) among the four subnetworks. Overlapping between the hubscore and z-score top most 100 genera (A), normalized abundance and participant coefficients (B), and all four subnetworks (C). (D) A heatmap showing the normalized abundance of all hub and connector genera in the Spu, Sps, F1, and F2 samples.
Figure 6
Figure 6
Taxonomy tree of the identified taxa based on the pitcher metatranscriptome alignment to proteins. (A) Metatranscripts of variable lengths aligned to the protein MAG TPA: carbamoyl-phosphate synthase large subunit (Sphingobacterium sp.). The vertical gray lines represent gaps. (B) The taxonomy tree of the identified taxa. The circles represent the log scale of number of metatranscripts assigned to the tree nodes and leaves. The numbers listed after each taxon name is the number of metatranscripts mapped to the proteins of this taxon.
Figure 7
Figure 7
The pitcher metatranscriptome: the abundant genera and proteins showing species-related patterns. (A) heatmap showing the TMM normalized abundance of the genera in the samples of Spu, Sps, F1, and F2 (p-values < 0.05). (B) similar to “A” but showing the abundance of the 25 protein with lowest P-values.
Figure 8
Figure 8
Function enrichment of the genotype-enriched metaproteins against the Go functional categories, uniprot keywords, STRING functional lists of Acidobacteria. The number of genes, FDR and fold enrichment of the significantly enriched functional categories in Spu, Sps, F1, and F2 metatranscriptomes are shown in (A-D), respectively.
Figure 9
Figure 9
Classification of the major function categories of the pitcher microbiome based on the number of metatranscripts mapped to PGPT ontology. The circles represent the log scale of number of metatranscripts assigned to each function. The number following each function is the number of metatranscripts mapped to this function.
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References

    1. Adlassnig W., Peroutka M., Lendi T. (2011). Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities. Ann. Bot. 107, 181–194. doi: 10.1093/aob/mcq238 - DOI - PMC - PubMed
    1. Afridi M. S., Ali S., Salam A., César Terra W., Hafeez A., Sumaira, et al. . (2022). Plant microbiome engineering: hopes or hypes. Biol. (Basel) 11, 1782. doi: 10.3390/biology11121782 - DOI - PMC - PubMed
    1. Agarwal P., Giri B. S., Rani R. (2020). Unravelling the role of rhizospheric plant-microbe synergy in phytoremediation: A genomic perspective. Curr. Genomics 21, 334–342. doi: 10.2174/1389202921999200623133240 - DOI - PMC - PubMed
    1. Albert V. A., Williams S. E., Chase M. W. (1992). Carnivorous plants: phylogeny and structural evolution. Science 257, 1491–1495. doi: 10.1126/science.1523408 - DOI - PubMed
    1. Anderson M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46. doi: 10.1111/j.1442-9993.2001.01070.pp.x - DOI

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