Spatio-temporal dynamics of sulfur bacteria during oxic--anoxic regime shifts in a seasonally stratified lake

Abstract

Sulfate-reducing bacteria (SRB) and sulfur-oxidizing bacteria drive major transformations in the sulfur cycle, and play vital roles in oxic--anoxic transitions in lakes and coastal waters. However, information on the succession of these sulfur bacteria in seasonally stratified lakes using molecular biological techniques is scarce. Here, we used 16S rRNA gene amplicon sequencing to study the spatio-temporal dynamics of sulfur bacteria during oxic--anoxic regime shifts in Lake Vechten. Oxygen and sulfate were mixed throughout the water column in winter and early spring. Meanwhile, SRB, green sulfur bacteria (GSB), purple sulfur bacteria (PSB), and colorless sulfur bacteria (CSB) exclusively inhabited the sediment. After the water column stratified, oxygen and nitrate concentrations decreased in the hypolimnion and various SRB species expanded into the anoxic hypolimnion. Consequently, sulfate was reduced to sulfide, stimulating the growth of PSB and GSB in the metalimnion and hypolimnion during summer stratification. When hypoxia spread throughout the water column during fall turnover, SRB and GSB vanished from the water column, whereas CSB (mainly Arcobacter) and PSB (Lamprocystis) became dominant and oxidized the accumulated sulfide under micro-aerobic conditions. Our results support the view that, once ecosystems have become anoxic and sulfidic, a large oxygen influx is needed to overcome the anaerobic sulfur cycle and bring the ecosystems back into their oxic state.

Figure 1.

Spatio-temporal dynamics of environmental variables in Lake Vechten. (A) Temperature; (B) dissolved oxygen; (C) sulfate; (D) sulfide.

Figure 2.

Dynamics of euphotic depth (Z_eu) and bacterial euphotic depth (B_eu) in Lake Vechten.

Figure 3.

Spatio-temporal dynamics of sulfur bacteria (genus level) in the water column of Lake Vechten, based on 16S rRNA gene amplicon sequences. The graphs show the relative abundances (%) and distributions of the sulfate-reducing bacteria (A) Desulfobulbus and (B) Desulfovibrio, the green sulfur bacteria (C) unknown Chlorobiaceae and (D) Chlorobium, the purple sulfur bacteria (E) Thiodictyon and (F) Lamprocystis, and the colorless sulfur bacteria (G) Arcobacter and (H) Sulfurimonas.

Figure 4.

Spatio-temporal dynamics of the relative abundances of sulfur bacteria in the sediment of Lake Vechten, based on 16S rRNA gene amplicon sequences.

Figure 5.

Redundancy analysis of the effect of environmental variables on the taxonomic composition of sulfur bacteria in the water column. The response variables (red arrows) were the relative abundances of sulfur bacteria. To avoid many zeroes in the data, we used only genera that were present in at least 15 water samples. Squares represent the samping points (yellow = spring; orange = summer; cyan = fall; green = winter). Total variation explained by the RDA model was 35.1%.

Figure 6.

Conceptual model of the seasonal dynamics of sulfur bacteria in the water column and sediment of Lake Vechten. The model shows the seasonal stratification and oxygen conditions. Line indicates the bacterial euphotic depth. The circles represent the different functional groups (colors) and genera (numbers). Grey circles represent sulfate-reducing bacteria (1, Desulfobulbus; 2, Desulfovibrio; 3, Desulfobacterium; 4, unknown Desulfobacteraceae; 5, Desulfuromonas; 6, Desulfomonile), purple circles represent purple sulfur bacteria (7, Thiodyction; 8, Lamprocystis; 9, Thiocystis; 10, Thiorhodococcus), green circles represent green sulfur bacteria (11, unknown Chlorobiaceae; 12, Chlorobium) and white circles represent colorless sulfur bacteria (13, Arcobacter; 14, Sulfurimonas; 15, Thiobacillus). The size of the circles gives a rough indication of the relative abundances of the different bacteria.