Evidence for possible syntrophic association of nitrifiying bacteria with Beggiatoa mats in hydrothermal vent sediments in the Guaymas Basin
Deep sea hydrothermal sediments found in the Guaymas Basin (Gulf of California) are carpeted with thick microbial mats characterised by Beggiatoa - a filamentous species of nitrate-respiring, sulfide-oxidising bacteria. These mats are fuelled by hydrothermal fluids, rich in ammonium, that mix below the surface and percolate up through the sediment where they cool before entering the water column. The high ammonium concentration in the fluids suggests it is likely to be an important energy source for chemoautotrophic interactions, not only within the hydrothermal vent plumes but also in the surrounding sediments.
Beggiatoa is punctuated with vacuoles, known to accumulate and store nitrate up to 4,000 times the ambient concentration. Due to the mats being at the interface of the oxic water column and cooled ammonium-rich vent fluids, mats such as these are hypothesised to be hotspots for nitrogen cycling. Prior to this study, anaerobic ammonia oxidation (anammox) is the only process that has been identified in these deep sea sulphur mats. The authors of this paper used both molecular and biochemical methods to assess whether nitrification was occurring.
O2, nitrogen oxide, nitrate & ammonium concentrations were measured both in situ, using microsensors and ship-board using washed and homogenised Beggiatoa mats, non-hydrothermal sediments free from ammonium and seawater taken 1m above the hydrothermal sediment surface. Using 15N-labelled ammonium chloride, linear nitrate formation was measured to estimate nitrification rates at between 370 and 920 times higher than the ambient seawater sample and up to 2000 times greater than that associated with non-hydrothermal sediments.
Quantitative PCR (qPCR) techniques were used to ascertain the copy number of the amoA gene of bacterial and archaeal ammonia-oxidisers, which encodes for the ammonia mono-oxidase subunit A. Presence of archaeal amoA gene copies were an order of magnitude higher within the
microbial mats than in the seawater sample and β-proteobacterial amoA was found in high concentrations in the mats but absent from the seawater. Microbial diversity was assessed using a gene library for AmoA sequences and the composition for the mats was distinct from non-hydrothermal sediments, hydrothermal plumes and the seawater.
Thaumarchaeotes, which include the ammonia-oxidising archaea (AOA) were detected using catalysed reporter deposition, integrated with fluorescent in situ hybridisation (CARD-FISH), along with 16s rRNA pyrotag techniques. AOA were found to outnumber ammonia-oxidising bacteria (AOB) by 6-8:1 and were found attached to many of the Beggiatoa filaments. These results suggest that when oxygen is depleted within the Beggiatoa mats, the close coupling, along with the high nitrification rates, is suggestive of inorganic nitrogen cycling between the ammonium and nitrate, triggering detoxification and oxidation of sulphide. This process may reduce the loss of bio available nitrogen in the sediments and potentially contributes to a substantial proportion of chemoautotrophic processes occurring at hydrothermal sites.
Winkel, M., Beer, D., Lavik, G., Peplies, J., & Mußmann, M. (2013). Close association of active nitrifiers with Beggiatoa mats covering deep‐sea hydrothermal sediments. Environmental Microbiology. In Press