The Invasive Brazilian Pepper Tree (Schinus terebinthifolius) Is Colonized by a Root Microbiome Enriched With Alphaproteobacteria and Unclassified Spartobacteria

Abstract

Little is known about the rhizosphere microbiome of the Brazilian pepper tree (BP) - a noxious category 1 invasive plant inducing an enormous economic and ecological toll in Florida. Some invasive plants have been shown to drastically change the soil microbiome compared to other native plants. The rhizobacteria community structure of BP, two Florida native plants (Hamelia patens and Bidens alba) and bulk soils were characterized across six geographical sites. Although all 19 well-known and 10 poorly described phyla were observed in all plant rhizospheres, BP contained the least total bacterial abundance (OTUs) with a distinct bacteria community structure and clustering patterns differing significantly (pCOA and PERMANOVA) from the natives and bulk soil. The BP rhizosphere community contained the highest overall Proteobacteria diversity (Shannon's diversity 3.25) in spite of a twofold reduction in richness of the Gammaproteobacteria. Remarkably, the invasive BP rhizosphere was highly enriched with Alphaproteobacteria, dominated by Rhizobiales, including Rhodoplanes and Bradyrhizobiaceae. Also, the relative abundance of Spartobacteria under BP rhizosphere was more than twice that of native plants and bulk soil; featuring unique members of the family Chthoniobacteraceae (DA101 genus). The trend was different for the family Pedosphaerae in the phylum Verrucomicrobia where the abundance declined under BP (26%) compared to (33-66%) for the H. patens native plant and bulk soil. BP shared the lowest number of unique phylotypes with bulk soil (146) compared to the other native plants with bulk soil (B. alba - 222, H. patens - 520) suggestive of its capacity to overcome biotic resistance. Although there were no specific biomarkers found, taken together, our data suggests that the occurrence of key bacteria groups across multiple taxonomic ranks provides a somewhat consistent profile of the invasive BP rhizo-community. Furthermore, based on the observed prevalence of a bacteria group (Spartobacteria - Chthoniobacteraceae - DA101); we propose that they have a possible role in BP biology. Our results emphasize the need to further investigate the potential value of "unique phylotypes" in the rhizosphere relative to bulk soil as an ecological tool for monitoring plant-cover/invasion history; or even detecting exotic plants with invasion tendencies.

Keywords: Brazilian pepper tree; Spartobacteria; biotic resistance; invasive plant; microbiome; rhizosphere.

FIGURE 1

(A) Overall relative abundance of top five phyla observed throughout all plant types and bulk soil. (B) The distances from the average relative abundance of Proteobacteria taxa for each plant type (invasive S. terebinthifolius, native H. patens, and native B. alba) and bulk soil where positive values have a relative abundance higher than the average and negative values have a relative abundance lower than the average. S. terebinthifolius has higher relative abundances of members of the Alphaproteobacteria class including unclassified Rhodoplanes, Bradyrhizobiaceae, and Rhizobium species.

FIGURE 2

(A) The distances from the average relative abundance of Verrucomicrobia taxa for each plant type (invasive S. terebinthifolius, native H. patens, and native B. alba) and bulk soil where positive values have a relative abundance higher than the average and negative values have a relative abundance lower than the average. The DA101 and Ellin515 unclassified Genus was more prevalent under S. terebinthifolius than the other native plants and bulk soil. (B) The distances from the average relative abundance of Acidobacteria taxa for each plant type (invasive S. terebinthifolius, native H. patens, and native B. alba) and bulk soil where positive values have a relative abundance higher than the average and negative values have a relative abundance lower than the average. In the rhizosphere of S. terebinthifolius the unclassified genus Koribacteraceae and Ellin6513 family are found predominantly compared to the native plants and bulk soil.

FIGURE 3

(A) Boxplots of phylum-specific OTU alpha diversity (Shannon’s index) from three phyla most dominant under the different plant types (S. terebinthifolius – ST, B. alba – BA, H. patens – HP) and bulk soil across the six sites. Shannon’s index computed using OTU counts in the vegan R package. (B) Beta-diversity pCoA weighted UniFrac plot of the different plant types and sites showing the community structure relationships of S. terebinthifolius, B. alba, H. patens, and bulk soil. Sites 2, 5, and 6 from S. terebinthifolius did not cluster together.

FIGURE 4

Number of shared phylotypes observed between (A) plant types [S. terebinthifolius – ST (n = 6), H. patens – HP (n = 6), B. alba – BA (n = 5), and bulk soil (n = 5)] and (B) three South Florida counties across the six sampling sites.