Eat it if you can

Published in Chemistry
Eat it if you can
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The Guaymas Basin is a hydrothermally active area in the Gulf of California, with thick, organic-rich sediments1 that exhibit diverse subseafloor temperature profiles. These hydrothermal sediments host a large range of hydrocarbons typically found in relic fuels (e.g., petroleum/crude oil). Hydrocarbons are compounds that contain carbon and hydrogen atoms, and in Guaymas Basin are found in mixed/complex pools containing saturated forms (single chemical bonds between the carbon atoms), aromatic molecules (contain one or more aromatic rings) and alkylated aromatic compounds, where the hydrogen atom(s) is/are replaced by alkyl-groups 2. Formation of these hydrocarbon cocktails in Guaymas Basin is enhanced by pyrolysis, a process whereby the sedimentary organic matter is rapidly transformed by hot hydrothermal fluids into hydrocarbons under high pressure and temperature (200-300oC) 3. The formed hydrocarbons can then migrate along hydrothermal flow paths and eventually emerge at the Guaymas seafloor in hydrocarbon-soaked sediment patches 4.  

Aside from their use in urban life, hydrocarbons can be also used by some naturally-occurring microbes that can utilize (degrade) hydrocarbons under a variety of aerobic (with oxygen) and anaerobic (no oxygen) conditions for energy gain 5. Nonetheless, the susceptibility of hydrocarbons to microbial degradation varies; the most easily attacked/utilized hydrocarbons are linear alkanes (carbon-to-carbon single bonds) followed by increasingly recalcitrant branched alkanes (branches of carbon atoms attached to the hydrocarbon chain), small monoaromatic hydrocarbons (contain only one aromatic ring), and finally polyaromatic hydrocarbons (PAHs) that contain multiple aromatic rings in their molecular structure 6. Guaymas sediments contain all these possible hydrocarbon combinations, and provide an excellent opportunity to investigate microbial hydrocarbon biodegradation because the Guaymas microbiota have had time to adapt to the hydrocarbon repertoire present 4.

The origin of, and microbial degradation of hydrocarbons in Guaymas Basin have been examined previously (7, 8 and references there in). In our study we used gas chromatography (GC-FID and GC-MS) to provide an extensive assessment of ~200 hydrocarbon compounds in porewaters and sediment cakes from AUV (autonomous underwater vehicle) Alvin pushcores, from three distinct hydrothermal areas located at the Guaymas Basin (Cathedral Hill, Aceto Balsamico and Marker 14) and we discuss their distribution and fate. We coupled these data with in-depth two-dimensional chromatography (GCxGC) to investigate specific signatures of microbial degradation of hydrocarbons at the two sites with the most contrasting GC-FID and GC-MS profiles (Cathedral Hill vs. Marker 14). These two sites have distinct temperature profiles (~21oC Cathedral Hill vs. > 70oC Maker 14 at 20 cm sediment depth) and overall geochemistry that includes higher acetate concentrations at the hot vs. the temperate sites 9.  We provide information on predominant biomarkers (molecules formed by microbial activity during microbial hydrocarbon degradation) such as hopanes and steranes, their analogues (e.g., diasteranes, mono-/tria-aromatic steranes), and what controls their distribution/fate in the sediments of these two contrasting sites (Figure 1).

Figure 1. The Cathedral Hill site (4991) and Marker 14 (4998) sites are covered with white, yellow and orange mats of sulfur-oxidizing bacterial mats (Beggiatoaceae). The two sites differ by temperature gradient. Scale bars are 10 cm based on Alvin’s laser beam scaler and the diameter of Alvin pushcores. Courtesy of Andreas Teske, U. North Carolina, Chapel Hill/NSF/AUV Sentry/2016 ©Woods Hole Oceanographic Institution.

Our data show that within the top centimeters of hydrothermal sediment (0-10 cm), biomarkers experience rapid alteration in Guaymas Basin. We find that the in situ sulfur-rich Guaymas conditions allow diagenetic alterations/oxidations of identified biomarkers to functionalized derivatives (e.g., aromatization of steranes to di/triaromatic steranes, and demethylation of hopanes to hopanoids) (Figure 2). Nonetheless, we detect distinct vertical distribution of specific biomarkers and biomarker-derivatives between the temperate Cathedral Hill and hot Marker 14 sites (Figure 3).

Figure 2. Overview of hopane and sterane biodegradation and oxidation pathways in Guaymas Basin organic rich sediments. Blue arrows indicate microbial biodegradation transforming hopanoids to sesquiterpanes, and red arrows indicate abiotic oxidation to form aromatized hopanoid and steroid compounds. Conceptual model provided by Robert K Nelson.

Figure 3. GCxGC-HRT chromatograms showing the downcore distribution of drimane/homodrimane (biomarkers of hopane microbial degradation) at different sediment depths in Cathedral Hill (left; core 4991-7) and Marker 14 (right; core 4998-15). Microbial degradation of hydrocarbons and abiotic hydrothermal flushing can co-exist, particularly in surficial sediments. With yellow the presence of microorganisms.

At our temperate site (21oC; Cathedral Hill) the detected biomarkers/biomarker-derivatives can be present throughout the investigated sediment depths. In contrast, at the hot site (> 50oC; Marker 14) these biomarkers exist primarily in the surficial sediment (0-7 cm) and disappear rapidly below the surface. It seems that in the hot, highly active hydrothermal sediments, the entire suite of biomarkers and their alteration products is shifted upwards and concentrated in the surface. This implies potential hydrothermal flushing of the biomarkers from the deeper sediment depths to the surface, as has been known to occur for sedimentary organic matter in the Guaymas Basin 10.

The same hydrothermal factors that concentrate hydrocarbons and biomarkers towards the sediment surface also impact the distribution, abundance and activities of microorganisms in Guaymas Basin sediments. The near-surface maximum microbial density 11 suggests microbial hydrocarbon and biomarker degradation would occur predominantly in surficial sediments where temperatures are not inhibiting microbial growth and activity, and where microbes can compete with, and/or complement abiotic processes such as hydrothermal flushing. Consistent with this notion, the surficial sediments of Guaymas Basin continue to generate discoveries of unusual hydrocarbon-degrading bacteria and archaea and they provide an attractive model system for exploring the microbial mechanisms, pathways and agents of hydrocarbon degradation in compound- and microbe-specific detail.

For details, please see our manuscript: https://www.nature.com/articles/s43247-022-00582-8

References:

  1. Calvert SE (1966). Accumulation of diatomaceous silica in the sediments of the Gulf of California. GSA Bulletin 77 (6): 569–596.
  2. Teske A (2020). Guaymas Basin, a Hydrothermal Hydrocarbon Seep Ecosystem. In: Teske A, Carvalho V (eds) Marine Hydrocarbon Seeps. Springer Oceanography. Springer, Cham.
  3. Kawka OE, Simoneit BRT (1994). Hydrothermal pyrolysis of organic matter in Guaymas Basin: I. Comparison of hydrocarbon distributions in subsurface sediments and seabed petroleums. Geochem. 22, 947–978.
  4. Edgcomb VP, Teske A., Mara P (2022). Microbial Hydrocarbon Degradation in Guaymas Basin—Exploring the Roles and Potential Interactions of Fungi and Sulfate-Reducing Bacteria. Microbiol. 13:831828.
  5. Leahy JG, Colwell RR. (1990). Microbial degradation of hydrocarbons in the environment. Microbiol Rev. 54(3):305-15.
  6. Das N, Chandran, P. 2011. Microbial degradation of petroleum hydrocarbon contaminants: an overview. Res. Internat: 941810.
  7. Simoneit BRT, Oros DR, Leif RN, Medeiros PM. (2019). Weathering and biodegradation of hydrothermal petroleum in the north rift of Guaymas Basin, Gulf of California. Revista Mexicana de Ciencias Geológicas, 36(2).
  8. Dalzell CJ, Ventura GT, Walters CC, Nelson RK, Reddy CM, Seewald JS., et al. (2021). Hydrocarbon transformations in sediments from the Cathedral Hill hydrothermal vent complex at Guaymas Basin, Gulf of California – A chemometric study of shallow seep architecture. Geochem. 152:104173.
  9. Zhuang GC, Montgomery A, Samarkin VA, Song M, Liu J, Schubotz F, et al. (2019). Generation and utilization of volatile fatty acids and alcohols in hydrothermally altered sediments in the Guaymas Basin, Gulf of California. Res. Lett. 46: 2637–2646.
  10. Lin YS, Koch B, Feseker T. et al. (2017). Near-surface heating of young rift sediment causes mass production and discharge of reactive dissolved organic matter. Rep. 7: 44864.
  11. Meyer S, Wegener G, Lloyd KG, et al. (2013). Microbial habitat connectivity across spatial scales and hydrothermal temperature gradients at Guaymas Basin. Front Microbiol. 4:207

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