Energetic and Environmental Constraints on the Community Structure of Benthic Microbial Mats in Lake Fryxell, Antarctica

Abstract

Ecological communities are commonly thought to be controlled by the dynamics of energy flow through environments. Two of the most important energetic constraints on all communities are photosynthetically active radiation (PAR) and oxygen concentration ([O 2 ]). Microbial mats growing on the bottom of Lake Fryxell, Antarctica, span environmental gradients in PAR and [O 2 ], which we used to test the extent to which each controls community structure. Metagenomic analyses showed variation in the diversity and relative abundances of Archaea, Bacteria, and Eukaryotes across three [O 2 ] and PAR conditions. Where [O 2 ] saturated the mats or was absent from the overlying water, PAR structured the community. Where [O 2 ] varied within mats, microbial communities changed across covarying PAR and [O 2 ] gradients. Diversity negatively correlated with [O 2 ] and PAR through mat layers in each habitat suggesting that, on the millimeter-scale, communities are structured by the optimization of energy use. In contrast, [O 2 ] positively correlated with diversity and affected the distribution of dominant populations across the three habitats, suggesting that meter-scale diversity is structured by energy availability. The benthic microbial communities in Lake Fryxell are thus structured by energy flow in a scale-dependent manner.

Environmental control on the distribution of metabolic strategies of benthic microbial mats in Lake Fryxell, Antarctica

“…At the mm-scale, phototrophs dominate top mat layers where they maximize conversion of PAR into chemical energy and suppress α-diversity due to their high population [23]. The phylogenetic diversity of the underlying non-phototrophic layers increases with depth into the mat, consistent with the maximum power principle, which predicts that communities are structured to optimize energy consumption over time [23,24]. In mat layers where [O 2 ] was saturating, PAR structured the community.…”

“…Specifically, microbial ecosystems in ice-covered lakes in the McMurdo Dry Valleys (MDVs), Antarctica, serve as natural laboratories to test the extent to which these models can explain community variations as a function of environmental gradients in photosynthetically active radiation (PAR) and oxygen concentration ([O 2 ]). The MDV lake environments are stable on decade-long timescales [20,21], containing well characterized PAR and slowly changing [O 2 ] gradients, which lead to predictable habitat heterogeneity [22,23]. PAR and [O 2 ] gradients are particularly prominent in Lake Fryxell, a perennially ice-covered, density-stratified lake in the Taylor Valley, Antarctica.…”

“…Our prior investigations into the relationships between the phylogenetic structure and taxonomic composition of Lake Fryxell's benthic microbial mats and local environmental conditions demonstrated that PAR and [O 2 ] affect local community membership differently at mmand m-scales [23]. At the mm-scale, phototrophs dominate top mat layers where they maximize conversion of PAR into chemical energy and suppress α-diversity due to their high population [23].…”

“…Our prior investigations into the relationships between the phylogenetic structure and taxonomic composition of Lake Fryxell's benthic microbial mats and local environmental conditions demonstrated that PAR and [O 2 ] affect local community membership differently at mmand m-scales [23]. At the mm-scale, phototrophs dominate top mat layers where they maximize conversion of PAR into chemical energy and suppress α-diversity due to their high population [23]. The phylogenetic diversity of the underlying non-phototrophic layers increases with depth into the mat, consistent with the maximum power principle, which predicts that communities are structured to optimize energy consumption over time [23,24].…”

“…Similarly, the stratification of lake water means that the transport of organisms within Lake Fryxell is likely too low for populations to be controlled by mass effects. Finally, since the landscape features (PAR, [O 2 ]) are heterogeneous, the patch dynamics model does not apply [23].…”