Microdiversity ensures the maintenance of functional microbial communities under changing environmental conditions

Abstract

Microdiversity can lead to different ecotypes within the same species. These are assumed to provide stability in time and space to those species. However, the role of microdiversity in the stability of whole microbial communities remains underexplored. Understanding the drivers of microbial community stability is necessary to predict community response to future disturbances. Here, we analyzed 16S rRNA gene amplicons from eight different temperate bog lakes at the 97% OTU and amplicon sequence variant (ASV) levels and found ecotypes within the same OTU with different distribution patterns in space and time. We observed that these ecotypes are adapted to different values of environmental factors such as water temperature and oxygen concentration. Our results showed that the existence of several ASVs within a OTU favored its persistence across changing environmental conditions. We propose that microdiversity aids the stability of microbial communities in the face of fluctuations in environmental factors.

Fig. 1

Detrended correspondence analysis (DCA) of the microbial community composition in OTUs and ASVs for the epilimnia and hypolimnia of the different lakes. Each point represents a sample. Lakes are indicated by point color. Procrustes analysis in the middle column shows the differences between the OTU and ASV-level ordinations

Fig. 2

Similarity decay plots for lakes NSB, TB, SSB, MA. Similarity in community composition over time for the four lakes sampled for 2 or more consecutive years. Boxplots show pairwise Bray–Curtis dissimilarities between samples, the x-axis shows time between sampling events

Fig. 3

ASVs from the same OTU show different habitat distributions. Distribution and habitat preference of four relevant OTUs, which are further discussed in the text. OTUs 1, 2, and 7 correspond to the ubiquitous freshwater clades PnecC, acI-B2, and bacI-A, while OTU-3 corresponds to a bloomer from the gamI clade. The radar charts show a the abundances (over 10,000 counts, logarithmic scale) and b z-scores of the three most abundant ASVs for each of the four OTUs. The colors of the inner-ring represent the mixing regime of the lake: green for polymictic, blue for dimictic, and red for meromictic. The shades of gray in the outer ring indicate the thermal layer (epilimnion and hypolimnion). Zero values have been plotted as log₁₀ (0.01). z-scores indicate the environmental preference of each ASV. Since the z-score normalization was made independently for each ASV, z-scores cannot be compared quantitatively among ASVs. The red dotted line indicates the mean abundance of each ASV, separating positive (white background) and negative (gray background) environmental preferences as schematically represented at the bottom right of the figure

Fig. 4

ASVs from the same OTU show different temporal dynamics in NSB. Both plots show the relative abundance of the 20 most abundant ASVs in each mixing layer and year and the relative abundance of the OTUs to which they belong to. Taxa were colored in gray except for OTU-1 and OTU-3, whose dynamics are discussed in detail in the main text. a Temporal abundance pattern of the most abundant persister OTU (OTU-1, PnecC clade), and its corresponding ecotypes with time. b Temporal abundance pattern of the most abundant bloomer OTU (OTU-3, gamI clade) and its corresponding ecotypes with time. In both cases, the middle row shows the temperature profiles along time and depth. Homogeneous vertical temperature profiles correspond to mixing events. In 2008, there was an artificial mixing event from 2^nd July to 10^th July, when homogeneous temperature was observed. Black vertical lines in the different panels indicate sampling points

Fig. 5

Effect of microdiversity on OTU persistence (top) and variability (bottom). Boxplots show the effect of microdiversity (left: low- vs. high-effective microdiversity; right: full range) in a the persistence and b the variability of OTUs. Significant (Welch’s t-test p < 0.001) differences between OTUs with low- and high-effective microdiversity are denoted with an asterisk. OTUs with a high-effective number of ASVs are indicated in the right part; their habitat distribution can be found in Fig. S6

Fig. 6

Microdiversity provides community stability across environmental gradients in freshwater ecosystems. a Freshwater model community proposed by García et al. [57]. b Amplicon sequence variants (ASVs) from the different member clades of the model community, classified according to their environmental preferences. c Relative abundance of low-temperature/oxygen (LTO) vs. high-temperature/oxygen (HTO) ecotypes of the model community in dimictic lake samples, plotted as a function of water temperature. Symbol color indicates dissolved oxygen concentration in shades of blue. Symbol shape indicates sampling year. Samples above the dashed red line are dominated by LTO ecotypes, and vice-versa. Significant linear regressions (FDR < 0.05) and 95% confidence intervals are shown with a red line and a shaded gray area, respectively