Methanogens and Their Syntrophic Partners Dominate Zones of Enhanced Magnetic Susceptibility at a Petroleum Contaminated Site

Abstract

Geophysical investigations documenting enhanced magnetic susceptibility (MS) within the water table fluctuation zone at hydrocarbon contaminated sites suggest that MS can be used as a proxy for investigating microbial mediated iron reduction during intrinsic bioremediation. Here, we investigated the microbial community composition over a 5-year period at a hydrocarbon-contaminated site that exhibited transient elevated MS responses. Our objective was to determine the key microbial populations in zones of elevated MS. We retrieved sediment cores from the petroleum-contaminated site near Bemidji, MN, United States, and performed MS measurements on these cores. We also characterized the microbial community composition by high-throughput 16S rRNA gene amplicon sequencing from samples collected along the complete core length. Our spatial and temporal analysis revealed that the microbial community composition was generally stable throughout the period of investigation. In addition, we observed distinct vertical redox zonations extending from the upper vadose zone into the saturated zone. These distinct redox zonations were concomitant with the dominant microbial metabolic processes as follows: (1) the upper vadose zone was dominated by aerobic microbial populations; (2) the lower vadose zone was dominated by methanotrophic populations, iron reducers and iron oxidizers; (3) the smear zone was dominated by iron reducers; and (4) the free product zone was dominated by syntrophic and methanogenic populations. Although the common notion is that high MS values are caused by high magnetite concentrations that can be biotically formed through the activities of iron-reducing bacteria, here we show that the highest magnetic susceptibilities were measured in the free-phase petroleum zone, where a methanogenic community was predominant. This field study may contribute to the emerging knowledge that methanogens can switch their metabolism from methanogenesis to iron reduction with associated magnetite precipitation in hydrocarbon contaminated sediments. Thus, geophysical methods such as MS may help to identify zones where iron cycling/reduction by methanogens is occurring.

Particle-associated and free-living microbial assemblages are distinct in a permanently redox-stratified freshwater lake

“…Notably, Methanoregula is often associated with particulate iron oxide (Beaver et al, 2016(Beaver et al, , 2021, as would be expected at these depths due to an active iron redox shuttle (Havig et al, 2015).…”

“…Methanogen composition appeared to be structured over depth by ambient geochemical conditions and possibly, competition with sulfate reducing bacteria for substrates (e.g., hydrogen, acetate). The only hydrogenotrophic methanogen ( Methanoregula , Beaver et al, 2016, 2021), was restricted to 20 and 20.5 m, where hydrogen sulfide concentrations, and presumably rates of microbial sulfate reduction are low. Notably, Methanoregula is often associated with particulate iron oxide (Beaver et al, 2016, 2021), as would be expected at these depths due to an active iron redox shuttle (Havig et al, 2015).…”

Microbially Induced Anaerobic Oxidation of Magnetite to Maghemite in a Hydrocarbon‐Contaminated Aquifer

“…The microbial communities in the study site are characterized by distinct vertical redox zonation. These distinct redox zonations and their corresponding microbial communities are discussed in detail in a recent study by Beaver et al (2021). These vertical zonations are depth zones defined by elevation measured in meters above sea level (masl), which include the upper vadose zone (UVZ; elevation >429 masl), lower vadose zone (LVZ; elevation between 425.5 to 429 masl), smear zone or water table fluctuation zone (WTFZ; elevation between 423.5 to 425.5 masl), and saturated zone (SZ; elevation <423.5 masl).…”

“…These vertical zonations are depth zones defined by elevation measured in meters above sea level (masl), which include the upper vadose zone (UVZ; elevation >429 masl), lower vadose zone (LVZ; elevation between 425.5 to 429 masl), smear zone or water table fluctuation zone (WTFZ; elevation between 423.5 to 425.5 masl), and saturated zone (SZ; elevation <423.5 masl). Here, we combine the smear zone and the free-product zone of Beaver et al (2021) to the WTFZ. Smithella was the dominant genus found in the free-phase oil zone followed by the hydrogenotrophic methanogen, Methanoregula.…”

“…Within the smear zone, the uncultured Coriobacteriaceae is the most dominant in the smear zone. Other microbial communities within the smear zone include Thermincola , Paenibacillus, and Beijerinckia (Beaver et al., 2021). The lower part of the smear zone is methanic and concomitant with observations of magnetic mineral enrichment and an increase in MS (Atekwana et al., 2014; Beaver et al., 2021; Lund et al., 2017).…”