Influence of Environmental Drivers and Potential Interactions on the Distribution of Microbial Communities From Three Permanently Stratified Antarctic Lakes

Abstract

The McMurdo Dry Valley (MDV) lakes represent unique habitats in the microbial world. Perennial ice covers protect liquid water columns from either significant allochthonous inputs or seasonal mixing, resulting in centuries of stable biogeochemistry. Extreme environmental conditions including low seasonal photosynthetically active radiation (PAR), near freezing temperatures, and oligotrophy have precluded higher trophic levels from the food webs. Despite these limitations, diverse microbial life flourishes in the stratified water columns, including Archaea, bacteria, fungi, protists, and viruses. While a few recent studies have applied next generation sequencing, a thorough understanding of the MDV lake microbial diversity and community structure is currently lacking. Here we used Illumina MiSeq sequencing of the 16S and 18S rRNA genes combined with a microscopic survey of key eukaryotes to compare the community structure and potential interactions among the bacterial and eukaryal communities within the water columns of Lakes Bonney (east and west lobes, ELB, and WLB, respectively) and Fryxell (FRX). Communities were distinct between the upper, oxic layers and the dark, anoxic waters, particularly among the bacterial communities residing in WLB and FRX. Both eukaryal and bacterial community structure was influenced by different biogeochemical parameters in the oxic and anoxic zones. Bacteria formed complex interaction networks which were lake-specific. Several eukaryotes exhibit potential interactions with bacteria in ELB and WLB, while interactions between these groups in the more productive FRX were relatively rare.

Keywords: McMurdo Dry Valley lakes; aquatic protists; environmental drivers; heterotrophic bacteria; interactions.

FIGURE 1

Vertical profiles of selected physicochemical and biological parameters within the lake water columns: East (A–C) and West (C–E) Lake Boney and Lake Fryxell (G–I). PAR, photosynthetically active radiation; DO, dissolved oxygen; SRP, soluble reactive phosphorus; DIC, dissolved inorganic carbon; Chl-a, chlorophyll a. Data points and bars in C, F and I represent mean ± range (n = 2) of cell counts. Bars are not visible when variation between replicates are smaller than the size of the data symbols.

FIGURE 2

Phylogenetic and morphological diversity of microbial eukaryotes communities residing in the water columns of the east and west lobes of Lake Bonney (ELB and WLB, respectively) and Lake Fryxell (FRX). (A) Phylogenetic diversity based on 18S rRNA gene sequences integrated within the whole water column of individual lakes. (B–M) Representative SEMs of key protists residing in the MDV lakes. B, Haptophyta, Isochrysis sp. (ELB,WLB); C, Chlorophyta, Chlamydomonas sp. (ELB, WLB); D, Chlorophyta, prasinophyte (ELB); E, Dinozoa (ELB); F, Cryptophyta, Geminigera sp. (FRX); G, Ciliophora, Euplotes sp. (FRX); H–J, Choanozoa (ELB, WLB); K,M, Ochrophyta, Chrysophytes (ELB, WLB); L, Personiomycota, Personia, sp. (ELB, WLB).

FIGURE 3

Diversity of Eukarya (A–C) and Bacteria (D–F) in the east and west lobes of Lake Bonney (ELB and WLB, respectively) and Lake Fryxell (FRX). The counts of OTUs based on 16S and 18S rRNA gene sequences are binned to phylum level, except for Proteobacteria which are shown in families. Light blue shows perennial ice covers and light gray indicates the permanent chemoclines in each lake.

FIGURE 4

(A) A non-metric multidimensional scaling (NMDS) plot of eukaryotic communities (OTU counts, Bray-Curtis dissimilarity, stress = 0.077). Shaded areas indicate 90% similarity within each lake. Shallow: epilimnion. Deep: chemocline + hypolimnion. (B) A NMDS plot of bacterial communities (OTU counts, Bray-Curtis dissimilarity, stress = 0.072). Oxic and anoxic: upper oxic zone and deep anoxic zone in the water columns, respectively. Shaded areas indicate 75% similarity within each lake.

FIGURE 5

Canonical correspondence analysis (CCA) plots showing corresponding relations between eukaryal (A) and bacterial (B) communities to physicochemical and biological factors in the east and west lobes of Lake Bonney (ELB and WLB, respectively) and Lake Fryxell (FRX). Shallow: epilimnion; Deep: chemocline + hypolimnion. Oxic and anoxic: upper oxic zone and deep anoxic zone in the water columns, respectively. TEMP, temperature; COND, conductivity; PAR, photosynthetically active radiation; NH₄, ammonium; NO₃, nitrate and nitrite; NP, N:P ratio; DO, dissolved oxygen; SRP, soluble reactive phosphorus; DIC, dissolved inorganic carbon; Chl, chlorophyll a. Algal abundance: CHLORO, chlorophytes; CRYPTO, cryptophytes; CHOANO, choanoflagellates; DINO, dinoflagellates; HAPTO, haptophytes. Bacterial abundance: Alpha, Alphaproteobacteria; Beta, Betaproteobacteria; Gamma, Gammaproteobacteria; Delta, Deltaproteobacteria; Actino, Actinobacteria; Bact, Bacteroidetes; Firm, Firmicutes; Planct, Planctomycetes; Verruco, Verrucomicrobia.

FIGURE 6

Co-occurrence patterns of OTUs in Lakes Bonney and Fryxell based on pairwise Pearson correlation coefficient between samples. (A) Co-occurrence between Eukarya and Bacteria in Lake Bonney. (B) Bacteria in Lake Bonney oxic zone. (C) Bacteria in Lake Bonney Anoxic zone. (D) Co-occurrence between Eukarya and Bacteria in Lake Fryxell. (E) All bacterial OTUs in Lake Fryxell. Nodes represent individual OTUs. Node colors represent phyla. The size of each node represents relative abundance of the corresponding OTU. Thickness of the circle outside each note indicates number of edges of corresponding note. Taxonomies of nodes were summarized in Supplementary Table S3.