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. 2010 Mar;76(6):1851-60.
doi: 10.1128/AEM.02440-09. Epub 2010 Jan 22.

The carnivorous pale pitcher plant harbors diverse, distinct, and time-dependent bacterial communities

Margaret M Koopman  1 , Danielle M Fuselier, Sarah Hird, Bryan C Carstens
Affiliations

The carnivorous pale pitcher plant harbors diverse, distinct, and time-dependent bacterial communities

Margaret M Koopman et al. Appl Environ Microbiol. 2010 Mar.

Abstract

The ability of American carnivorous pitcher plants (Sarracenia) to digest insect prey is facilitated by microbial associations. Knowledge of the details surrounding this interaction has been limited by our capability to characterize bacterial diversity in this system. To describe microbial diversity within and between pitchers of one species, Sarracenia alata, and to explore how these communities change over time as pitchers accumulate and digest insect prey, we collected and analyzed environmental sequence tag (454 pyrosequencing) and genomic fingerprint (automated ribosomal intergenic spacer analysis and terminal restriction fragment length polymorphism) data. Microbial richness associated with pitcher plant fluid is high; more than 1,000 unique phylogroups were identified across at least seven phyla and 50 families. We documented an increase in bacterial diversity and abundance with time and observed repeated changes in bacterial community composition. Pitchers from different plants harbored significantly more similar bacterial communities at a given time point than communities coming from the same genetic host over time. The microbial communities in pitcher plant fluid also differ significantly from those present in the surrounding soil. These findings indicate that the bacteria associated with pitcher plant leaves are far from random assemblages and represent an important step toward understanding this unique plant-microbe interaction.

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Figures

FIG. 1.
FIG. 1.
Microbial diversity in Sarracenia alata pitcher fluid at different taxonomic ranks. Degree of overlap between 454 sequence data (large white boxes) and ARISA fragment data (large gray boxes) at the level of phylum, class, order, and family. The number in each small box indicates the number of sequences in that particular group, and black boxes indicate that the group was unidentifiable at that rank.
FIG. 2.
FIG. 2.
Rarefaction analysis of 454 sequence data at 3 and 7% divergence. Chao 1 estimates suggest 1,033.94 phylogroups at 0.03 divergence and 298.76 at 0.07 divergence.
FIG. 3.
FIG. 3.
Species accumulation curves for ARISA and T-RFLP data for all pitchers over 5 months (smooth lines) and for April only (lines with symbols). A curve is also estimated for fragments from soil over 5 months (broken line). ARISA data from fluid indicate 485 unique fragment sizes; the Chao 1 estimate for these data estimates a total of 574. All T-RFLP data indicate a total of 56 unique peaks; Chao 1 for these data estimates a total of 112.
FIG. 4.
FIG. 4.
Frequency distribution of fragment lengths in the ARISA and T-RFLP pitcher fluid data sets over all sampling time points.
FIG. 5.
FIG. 5.
Abundance and diversity in peak number for fingerprinting data over sampling season. Peak abundance (total) is provided for ARISA (fluid and soil) and T-RFLP data, and peak diversity (unique) is provided for ARISA data (fluid and soil). Pitcher fluid was not sampled in March, since pitchers opened in March and were sterile (0 bacteria) at the time of opening (dotted lines originating at 0 in March represent an increase in bacteria since opening).
FIG. 6.
FIG. 6.
Number of peaks found in more than 50% of sampled pitchers within each month according to ARISA (fluid and soil) data. Two environmental measures (average temperature by month and precipitation in inches) are also plotted.
FIG. 7.
FIG. 7.
Distribution of shared ARISA peaks in pitcher fluid over time. Colors indicate the number of shared peaks over a range of consecutive months. For example, 18 peaks are shared in all 5 months. The most shared peaks are found in months with the highest bacterial abundance and diversity (June and July).
FIG. 8.
FIG. 8.
Multidimensional scaling ordination of ARISA fluid data coded by month. Each point represents the bacterial community from one pitcher.
FIG. 9.
FIG. 9.
Similarity dendrogram using Bray-Curtis similarities, highlighting the difference in composition of the microbial communities present in soil samples and pitcher samples over the 5-month sampling regimen.
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