Carbon metabolism and adaptation of hyperalkaliphilic microbes in serpentinizing spring of Manleluag, the Philippines

Wang, Yong; Li, Wenli; Baker, Brett J.; Zhou, Yingli; He, Lisheng; Danchin, Antoine; Li, Qingmei; Gao, Zhaoming

doi:10.1111/1758-2229.13052

Cited by 4 publications

(1 citation statement)

References 57 publications

(93 reference statements)

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“…Sites of terrestrial serpentinization are distributed globally and show evidence of methanogenic and methanotrophic microbial members, including the Voltri Massif (Italy), Santa Elena Ophiolite (Costa Rica), the Chimaera Seeps (Turkey), and the Manleluag Spring National Park of Zamabales (Philippines; Brazelton et al, 2017 ; Crespo-Medina et al, 2017 ; Zwicker et al, 2018 ; Wang et al, 2022 ). Specifically, the Samail Ophiolite, Sultanate of Oman, offers the largest exposed ophiolite on Earth that is actively undergoing low temperature serpentinization ( Neal and Stanger, 1985 ; Kelemen and Matter, 2008 ; Kelemen et al, 2011 ; Paukert et al, 2012 ; Miller et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Metapangenomic investigation provides insight into niche differentiation of methanogenic populations from the subsurface serpentinizing environment, Samail Ophiolite, Oman

et al. 2023

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Serpentinization reactions produce highly reduced waters that have hyperalkaline pH and that can have high concentrations of H2 and CH4. Putatively autotrophic methanogenic archaea have been identified in the subsurface waters of the Samail Ophiolite, Sultanate of Oman, though the strategies to overcome hyperalkaline pH and dissolved inorganic carbon limitation remain to be fully understood. Here, we recovered metagenome assembled genomes (MAGs) and applied a metapangenomic approach to three different Methanobacterium populations to assess habitat-specific functional gene distribution. A Type I population was identified in the fluids with neutral pH, while a Type II and “Mixed” population were identified in the most hyperalkaline fluids (pH 11.63). The core genome of all Methanobacterium populations highlighted potential DNA scavenging techniques to overcome phosphate or nitrogen limitation induced by environmental conditions. With particular emphasis on the Mixed and Type II population found in the most hyperalkaline fluids, the accessory genomes unique to each population reflected adaptation mechanisms suggesting lifestyles that minimize niche overlap. In addition to previously reported metabolic capability to utilize formate as an electron donor and generate intracellular CO2, the Type II population possessed genes relevant to defense against antimicrobials and assimilating potential osmoprotectants to provide cellular stability. The accessory genome of the Mixed population was enriched in genes for multiple glycosyltransferases suggesting reduced energetic costs by adhering to mineral surfaces or to other microorganisms, and fostering a non-motile lifestyle. These results highlight the niche differentiation of distinct Methanobacterium populations to circumvent the challenges of serpentinization impacted fluids through coexistence strategies, supporting our ability to understand controls on methanogenic lifestyles and adaptations within the serpentinizing subsurface fluids of the Samail Ophiolite.

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Section: Introductionmentioning

confidence: 99%

Metapangenomic investigation provides insight into niche differentiation of methanogenic populations from the subsurface serpentinizing environment, Samail Ophiolite, Oman

et al. 2023

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Microbial survival mechanisms within serpentinizing Mariana forearc sediments

Mullis

Selwyn

Kevorkian

et al. 2023

FEMS Microbiology Ecology

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Marine deep subsurface sediment is often a microbial environment under energy-limited conditions. However, microbial life has been found to persist and even thrive in deep subsurface environments. The Mariana forearc represents an ideal location for determining how microbial life can withstand extreme conditions including pH 10–12.5 and depleted nutrients. The International Ocean Discovery Program Expedition 366 to the Mariana Convergent Margin sampled three serpentinizing seamounts located along the Mariana forearc chain with elevated concentrations of methane, hydrogen, and sulfide. Across all three seamount summits, the most abundant transcripts were for cellular maintenance such as cell wall and membrane repair, and the most abundant metabolic pathways were the Entner-Doudoroff pathway and tricarboxylic acid cycle. At flank samples, sulfur cycling involving taurine assimilation dominated the metatranscriptomes. The in situ activity of these pathways was supported by the detection of their metabolic intermediates. All samples had transcripts from all three domains of Bacteria, Archaea, and Eukarya, dominated by Burkholderiales, Deinococcales, and Pseudomonales, as well as the fungal group Opisthokonta. All samples contained transcripts for aerobic methane oxidation (pmoABC) and denitrification (nirKS). The Mariana forearc microbial communities show activity not only consistent with basic survival mechanisms, but also coupled metabolic reactions.

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The Microbial Ecology of Serpentinites

Colman,

Templeton,

Spear

et al. 2024

Preprint

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Serpentinization, the collective set of geochemical reactions initiated by the hydration of ultramafic rock, has occurred throughout Earth history and is inferred to occur on several planets and moons in our solar system. These reactions generate highly reducing conditions that can drive organic synthesis reactions potentially conducive to the emergence of life, while concomitantly generating fluids that are challenging for life owing to hyperalkalinity and limited inorganic carbon (and oxidant) availability. Consequently, serpentinite-hosted biospheres offer insights into the earliest life, the habitable limits for life, and the potential for life on other planets. However, the ability of serpentinites to support abundant microbial communities was only recognized ~20 years ago with the discovery of deep-sea hydrothermal vents emanating serpentinized fluids. Here, we review the microbial ecology of marine and continental serpentinite-hosted biospheres in conjunction with a comparison of publicly available metagenomic sequence data from these communities to provide a global perspective of serpentinite ecology. Synthesis of observations across global systems reveal consistent themes in the diversity, ecology, and functioning of communities. Nevertheless, individual systems exhibit nuances due to local geology, hydrology, and input of oxidized, near-surface/seawater fluids. Further, several new (and old) questions remain including the provenance of carbon to support biomass synthesis, the physical and chemical limits of life in serpentinites, the mode and tempo of in situ evolution, and the extent to which modern serpentinites serve as analogs for those on early Earth. These topics are explored herein from a microbial perspective to outline key knowledge-gaps that should be a focus of future research.

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Carbon metabolism and adaptation of hyperalkaliphilic microbes in serpentinizing spring of Manleluag, the Philippines

Cited by 4 publications

References 57 publications

Metapangenomic investigation provides insight into niche differentiation of methanogenic populations from the subsurface serpentinizing environment, Samail Ophiolite, Oman

Metapangenomic investigation provides insight into niche differentiation of methanogenic populations from the subsurface serpentinizing environment, Samail Ophiolite, Oman

Microbial survival mechanisms within serpentinizing Mariana forearc sediments

The Microbial Ecology of Serpentinites

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