Microbial eukaryote plankton communities of high-mountain lakes from three continents exhibit strong biogeographic patterns

Abstract

Microbial eukaryotes hold a key role in aquatic ecosystem functioning. Yet, their diversity in freshwater lakes, particularly in high-mountain lakes, is relatively unknown compared with the marine environment. Low nutrient availability, low water temperature and high ultraviolet radiation make most high-mountain lakes extremely challenging habitats for life and require specific molecular and physiological adaptations. We therefore expected that these ecosystems support a plankton diversity that differs notably from other freshwater lakes. In addition, we hypothesized that the communities under study exhibit geographic structuring. Our rationale was that geographic dispersal of small-sized eukaryotes in high-mountain lakes over continental distances seems difficult. We analysed hypervariable V4 fragments of the SSU rRNA gene to compare the genetic microbial eukaryote diversity in high-mountain lakes located in the European Alps, the Chilean Altiplano and the Ethiopian Bale Mountains. Microbial eukaryotes were not globally distributed corroborating patterns found for bacteria, multicellular animals and plants. Instead, the plankton community composition emerged as a highly specific fingerprint of a geographic region even on higher taxonomic levels. The intraregional heterogeneity of the investigated lakes was mirrored in shifts in microbial eukaryote community structure, which, however, was much less pronounced compared with interregional beta-diversity. Statistical analyses revealed that on a regional scale, environmental factors are strong predictors for plankton community structures in high-mountain lakes. While on long-distance scales (>10 000 km), isolation by distance is the most plausible scenario, on intermediate scales (up to 6000 km), both contemporary environmental factors and historical contingencies interact to shift plankton community structures.

Keywords: alpine lakes; biogeography; diversity; fungi; next-generation sequencing; protistan plankton.

Fig.1

Shannon-based effective number of species (alpha-diversity) between the sampled lakes in the European Alps, the Chilean Altiplano and the Ethiopian Bale Mountains. Results are based on normalized data sets (n = 36 744).

Fig. 2

Distribution of the protistan and fungal communities among the analysed lakes in the European Alps, the Chilean Altiplano and the Ethiopian Bale Mountains. The bars display the relative number of distinct operational taxonomic units (OTUs) per taxonomic group (i.e. OTU richness). Only those taxonomic groups (phylum level) were considered that contain at least 1% of the total number of OTUs per sample.

Fig. 3

Nonmetric multidimensional scaling analysis of the European, Chilean and Ethiopian high-mountain lake samples under study based on Jaccard similarities. For each community cluster, the ellipses represent 95% confidence intervals.

Fig. 4

Relationship between the pairwise community (Sorensen distance) and geographic distances (log-transformed) for the analysed high-mountain lakes (including winter samples).

Fig. 5

Mantel correlogram displaying spatial structuring of the high-mountain lake communities within the following nonoverlapping distance classes: 0–50 km, 5235–5278 km and 10 741–12 270 km.

Fig. 6

Analyses of the novel diversity within the protistan (and fungal) communities in the European Alps lakes (a), the Chilean Altiplano lakes (b) and the Ethiopian Bale Mountain lakes (c). Each dot represents one operational taxonomic unit (OTU), the different colours indicate the level of sequence similarity to a deposited reference sequence, and the size of on OTU indicates the number of included V4 sequences. An edge weight (sequence similarity) of 90% was chosen to discriminate between the different OTUs.