Out of the dark: transitional subsurface-to-surface microbial diversity in a terrestrial serpentinizing seep (Manleluag, Pangasinan, the Philippines)

Abstract

In the Zambales ophiolite range, terrestrial serpentinizing fluid seeps host diverse microbial assemblages. The fluids fall within the profile of Ca2+-OH−-type waters, indicative of active serpentinization, and are low in dissolved inorganic carbon (DIC) (<0.5 ppm). Influx of atmospheric carbon dioxide (CO2) affects the solubility of calcium carbonate as distance from the source increases, triggering the formation of meter-scale travertine terraces. Samples were collected at the source and along the outflow channel to determine subsurface microbial community response to surface exposure. DNA was extracted and submitted for high-throughput 16S rRNA gene sequencing on the Illumina MiSeq platform. Taxonomic assignment of the sequence data indicates that 8.1% of the total sequence reads at the source of the seep affiliate with the genus Methanobacterium. Other major classes detected at the source include anaerobic taxa such as Bacteroidetes (40.7% of total sequence reads) and Firmicutes (19.1% of total reads). Hydrogenophaga spp. increase in relative abundance as redox potential increases. At the carbonate terrace, 45% of sequence reads affiliate with Meiothermus spp. Taxonomic observations and geochemical data suggest that several putative metabolisms may be favorable, including hydrogen oxidation, H2-associated sulfur cycling, methanogenesis, methanotrophy, nitrogen fixation, ammonia oxidation, denitrification, nitrate respiration, methylotrophy, carbon monoxide respiration, and ferrous iron oxidation, based on capabilities of nearest known neighbors. Scanning electron microscopy and energy dispersive X-ray spectroscopy suggest that microbial activity produces chemical and physical traces in the precipitated carbonates forming downstream of the seep's source. These data provide context for future serpentinizing seep ecosystem studies, particularly with regards to tropical biomes.

Geochemical bioenergetics during low‐temperature serpentinization: An example from the Samail ophiolite, Sultanate of Oman

“…In general, temperatures of all spring sources were elevated relative to air temperatures in January, possibly reflecting values closer to the average ambient temperature or possibly some heating from the geothermal gradient during circulation in the subsurface. The temperature and pH data obtained in this study fall within the ranges of previous studies [ Neal and Stanger , , ; Stanger , ; Boulart et al ., , ; Chavagnac et al ., ] and are in line with investigations of other hyperalkaline spring systems resulting from serpentinization [ Barnes et al ., ; Neal and Shand , ; Cipolli et al ., ; Boschetti and Toscani , ; Marques et al ., ; Boulart et al ., , ; Morrill et al ., ; Monnin et al ., , ; Cardace et al ., ; Woycheese et al ., ]. In general, as pH increases so do the concentrations of reduced species while those of oxidized species decrease.…”

“…The process of serpentinization has attracted considerable attention as a model for how planets support life without photosynthesis, leading to suggestions that water‐rock reactions within terrestrial planets, icy moons, and ocean worlds support microbial habitability in the dark [ Shock , ; Jakosky and Shock , ; McCollom , ; Zolotov and Shock , , ; Cardace and Hoehler , ; Edwards et al ., ]. On Earth, serpentinization yields novel habitats in continental and marine settings, featuring hyperalkaline pH (>11) and extremely reduced conditions [ Barnes et al ., ; Kelley et al ., , ; Salisbury et al ., ; Neal and Shand , ; Cipolli et al ., ; Proskurowski et al ., ; Fryer and Salisbury , ; Boschetti and Toscani , ; Marques et al ., ; Wheat et al ., , ; Lang et al ., ; Paukert et al ., ; Boulart et al ., , ; Morrill et al ., ; Monnin et al ., , ; Cardace et al ., ; Woycheese et al ., ; Miller et al ., ], and may be a mechanism for life to infiltrate deep into subduction zones. Arguments for the ultramafic nature of the crust and upper mantle of the early Earth lead to the suggestion that the emergence of life was hosted in serpentinizing systems [ Sleep et al ., , ; Russell , ; Martin et al ., ; Russell et al ., ; Lane et al ., ; Lane , , ; Lane and Martin , ; Sousa et al ., ; Herschy et al ., ; Martin et al ., ; Weiss et al ., ].…”

“…These Class V data can only be taken as suggestions of possible chemolithotrophic metabolisms until more solid evidence is developed. Nevertheless, they point to the possibility for CO oxidation [ Brazelton et al ., ], hydrogen oxidation [ Brazelton et al ., ; Suzuki et al ., ; Tiago and Veríssimo , ; Sánchez‐Murillo et al ., ; Quéméneur et al ., , ; Miller et al ., ], methanogenesis [ Brazelton et al ., ; Blank et al ., ; Sánchez‐Murillo et al ., ; Quéméneur et al ., , ; Baculi et al ., ; Woycheese et al ., ; Miller et al ., ], anaerobic methane oxidation [ Curtis et al ., ; Quéméneur et al ., , ; Miller et al ., ], nitrogen reduction [ Quéméneur et al ., ], sulfate reduction [ Brazelton et al ., ; Blank et al ., ; Tiago and Veríssimo , ; Curtis et al ., ; Quéméneur et al ., ; Postec et al ., ; Miller et al ., ], sulfide oxidation [ Quéméneur et al ., ], and ammonia oxidation [ Quéméneur et al ., , ; Baculi et al ., ]. In addition, Class V evidence for aerobic methanotrophy is offered by Sánchez‐Murillo et al .…”

“…• Data Set S18 • Data Set S19 Boschetti and Toscani, 2008;Marques et al, 2008;Wheat et al, 2008Wheat et al, , 2010Lang et al, 2010;Paukert et al, 2012;Boulart et al, 2012Boulart et al, , 2013Morrill et al, 2013;Monnin et al, 2014aMonnin et al, , 2014bCardace et al, 2015;Woycheese et al, 2015;Miller et al, 2016], and may be a mechanism for life to infiltrate deep into subduction zones. Arguments for the ultramafic nature of the crust and upper mantle of the early Earth lead to the suggestion that the emergence of life was hosted in serpentinizing systems [Sleep et al, 2004[Sleep et al, , 2011Russell, 2007;Martin et al, 2008;Russell et al, 2010;Lane et al, 2010;Lane, 2010Lane, , 2014Lane and Martin, 2012;Sousa et al, 2013;Herschy et al, 2014;Martin et al, 2014;Weiss et al, 2016].…”

In situ electrochemical enrichment and isolation of a magnetite‐reducing bacterium from a high pH serpentinizing spring

“…Serpentinizing systems are home to streamlined or low diversity/abundance microbial communities with characteristic taxa Suzuki et al, 2013;Tiago and Ver ıssimo, 2013;Mei et al, 2014;Meyer-Dombard et al, 2014;Woycheese et al, 2015). Although terrestrial sites in general contain less abundant populations and less diverse microbial communities than their marine counterparts (likely linked to the availability of terminal electron acceptors), there are common taxa observed at sites with similar geochemical profiles.…”