Impact of Seasonal Hypoxia on Activity and Community Structure of Chemolithoautotrophic Bacteria in a Coastal Sediment

Abstract

Seasonal hypoxia in coastal systems drastically changes the availability of electron acceptors in bottom water, which alters the sedimentary reoxidation of reduced compounds. However, the effect of seasonal hypoxia on the chemolithoautotrophic community that catalyzes these reoxidation reactions is rarely studied. Here, we examine the changes in activity and structure of the sedimentary chemolithoautotrophic bacterial community of a seasonally hypoxic saline basin under oxic (spring) and hypoxic (summer) conditions. Combined 16S rRNA gene amplicon sequencing and analysis of phospholipid-derived fatty acids indicated a major temporal shift in community structure. Aerobic sulfur-oxidizing Gammaproteobacteria (Thiotrichales) and Epsilonproteobacteria (Campylobacterales) were prevalent during spring, whereas Deltaproteobacteria (Desulfobacterales) related to sulfate-reducing bacteria prevailed during summer hypoxia. Chemolithoautotrophy rates in the surface sediment were three times higher in spring than in summer. The depth distribution of chemolithoautotrophy was linked to the distinct sulfur oxidation mechanisms identified through microsensor profiling, i.e., canonical sulfur oxidation, electrogenic sulfur oxidation by cable bacteria, and sulfide oxidation coupled to nitrate reduction by Beggiatoaceae. The metabolic diversity of the sulfur-oxidizing bacterial community suggests a complex niche partitioning within the sediment, probably driven by the availability of reduced sulfur compounds (H 2 S, S 0 , and S 2 O 3 2Ϫ ) and electron acceptors (O 2 and NO 3 Ϫ ) regulated by seasonal hypoxia.IMPORTANCE Chemolithoautotrophic microbes in the seafloor are dependent on electron acceptors, like oxygen and nitrate, that diffuse from the overlying water. Seasonal hypoxia, however, drastically changes the availability of these electron acceptors in the bottom water; hence, one expects a strong impact of seasonal hypoxia on sedimentary chemolithoautotrophy. A multidisciplinary investigation of the sediments in a seasonally hypoxic coastal basin confirms this hypothesis. Our data show that bacterial community structure and chemolithoautotrophic activity varied with the seasonal depletion of oxygen. Unexpectedly, the dark carbon fixation was also dependent on the dominant microbial pathway of sulfur oxidation occurring in the sediment (i.e., canonical sulfur oxidation, electrogenic sulfur oxidation by cable bacteria, and sulfide oxidation coupled to nitrate reduction by Beggiatoaceae). These results suggest that a complex niche partitioning within the sulfur-oxidizing bacterial

Assessing the metabolism of sedimentary microbial communities using the hydrogen isotopic composition of fatty acids

“…Therefore, the bacterial diversity of sediment cores taken in August was studied using 16S rRNA gene amplicon sequencing. The phylogenetic data for the first cm in both Stations 1 and 3 has been previously reported by Lipsewers et al (2017) and here we report data for depth interval of the first 8 cm. In order to assess only the bacterial reads, chloroplast reads were removed.…”

“…The decaying biomass of the summer bloom is thought to contribute to the hypoxia/anoxia in the water column during late summer (Hagens et al, 2015). Recently, the microbial community of the sulfidic sediment has been the topic of several studies (Malkin et al, 2014;Seitaj et al, 2015;Vasquez-Cardenas et al, 2015;Rao et al, 2016;Sulu-Gambari et al, 2016a;2016b;Lipsewers et al, 2016;2017). Desulfobulbaceae filaments capable of electrogenic sulfide oxidation (Malkin et al, 2014;Vasquez-Cardenas et al, 2015) and nitrate-accumulating Beggiatoaceae (Seitaj et al, 2015) have been shown to be present in the Den Osse Basin.…”

“…Furthermore, heterotrophic denitrifiers and anammox bacteria play a role in the nitrogen cycle in the sediments (Lipsewers et al, 2016). The seasonal shift from oxic to hypoxic/anoxic conditions leads to a community shift from chemoautotrophic Gamma-and Epsilonproteobacteria to sulfate reducing Deltaproteobacteria and a decrease in chemoautotrophic inorganic carbon fixation rates (Lipsewers et al 2017) Sediment cores were taken on board of the R/V Luctor in March and August 2012 at two different stations. Station 1 had a water depth of 34 m (51.747 ºN, 3.890 ºE) and station 3 had a water depth of 17 m (51.747 ºN, 3.898 ºE) (Hagens et al, 2015).…”

“…In order to further test the application of the D/H ratio of FAs as a tool to study microbial metabolism, we studied the D/H ratio of FAs of the microbial communities in surface sediments obtained from Lake Grevelingen, a marine influenced lake. We studied two different stations, a shallow station with oxic bottom water in spring (March) and hypoxic bottom water in summer (August) and a deep station with oxic bottom water in spring and anoxic bottom water in summer (Lipsewers et al, 2016;2017). This allows us to study spatial and seasonal differences in microbial metabolism due to changing oxygen concentrations.…”

Application of the isotope pairing technique in sediments: Use, challenges, and new directions

“…As discussed above, the presence of NO 3 − ‐storing organisms can pose a significant issue for the IPT. However the presence of these organisms may be transient, with seasonal studies noting the presence of Beggiatoa mats typically only during warmer months when the overlying water is hypoxic (Jäntti and Hietanen ; Bonaglia et al ; Sulu‐Gambari et al ; Lipsewers et al ). Accordingly, during certain months of the year it may be necessary to carry out additional NO 3 − storage experiments or calculations (e.g., Glud et al ; Song et al ).…”