Chemoautotrophic Carbon Fixation Rates and Active Bacterial Communities in Intertidal Marine Sediments

Abstract

Chemoautotrophy has been little studied in typical coastal marine sediments, but may be an important component of carbon recycling as intense anaerobic mineralization processes in these sediments lead to accumulation of high amounts of reduced compounds, such as sulfides and ammonium. We studied chemoautotrophy by measuring dark-fixation of 13C-bicarbonate into phospholipid derived fatty acid (PLFA) biomarkers at two coastal sediment sites with contrasting sulfur chemistry in the Eastern Scheldt estuary, the Netherlands. At one site where free sulfide accumulated in the pore water right to the top of the sediment, PLFA labeling was restricted to compounds typically found in sulfur and ammonium oxidizing bacteria. At the other site, with no detectable free sulfide in the pore water, a very different PLFA labeling pattern was found with high amounts of label in branched i- and a-PLFA besides the typical compounds for sulfur and ammonium oxidizing bacteria. This suggests that other types of chemoautotrophic bacteria were also active, most likely Deltaproteobacteria related to sulfate reducers. Maximum rates of chemoautotrophy were detected in first 1 to 2 centimeters of both sediments and chemosynthetic biomass production was high ranging from 3 to 36 mmol C m−2 d−1. Average dark carbon fixation to sediment oxygen uptake ratios were 0.22±0.07 mol C (mol O2)−1, which is in the range of the maximum growth yields reported for sulfur oxidizing bacteria indicating highly efficient growth. Chemoautotrophic biomass production was similar to carbon mineralization rates in the top of the free sulfide site, suggesting that chemoautotrophic bacteria could play a crucial role in the microbial food web and labeling in eukaryotic poly-unsaturated PLFA was indeed detectable. Our study shows that dark carbon fixation by chemoautotrophic bacteria is a major process in the carbon cycle of coastal sediments, and should therefore receive more attention in future studies on sediment biogeochemistry and microbial ecology.

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

“…Deltaproteobacteria, such as Desulfobacterium autotrophicum and Desulfocapsa sp., as identified by 16S rRNA gene sequencing, are known to grow as chemolithoautotrophs by performing H 2 oxidation or S 0 disproportionation (43,44) (Fig. 6) and are important contributors to the chemolithoautotrophic activity in coastal sediments (11,45). However, a further identification of the chemolithoautotrophic Deltaproteobacteria through the functional genes related to carbon fixation pathways was not performed in this study.…”

“…In March, stations S1 and S3 also showed a higher contribution of fatty acids occurring in the sulfate-reducing Deltaproteobacteria (11,36,42) than the PLFA-SIP profiles at station S2 (Fig. 3b).…”

“…Stock solutions of 80 mM [ 13 C]bicarbonate (99% 13 C; Cambridge Isotope Laboratories, Andover, MA, USA) were prepared as previously described (11). [ 13 C]Bicarbonate was added to the sediment from 3 cm above the surface to 8 cm deep in the sediment cores in aliquots of 100 l through vertically aligned side ports (0.5 cm apart) with the line injection method (58).…”

“…Pore water was obtained by centrifugation (4,500 rpm for 5 min) for dissolved inorganic carbon (DIC) analysis, and sediments were lyophilized for PLFA analysis. Biomarker extractions were performed on freeze-dried sediment, as described before (59) and 13 C incorporation into PLFA was analyzed as previously reported (11). Nomenclature of PLFA can be found in the supplemental material.…”

“…Both chemolithoautotrophic sulfur-oxidizing Gammaproteobacteria and sulfur-disproportionating Deltaproteobacteria have been identified to play a major role in sulfur and carbon cycling in diverse intertidal sediments (10)(11)(12). Hence, chemolithoautotrophic sulfur-oxidizing communities vary between sediment environments, but it is presently not clear as to which environmental factors are actually determining the chemolithoautotrophic community composition at a given site.…”