Seafloor incubation experiments at deep-sea hydrothermal vents reveal distinct biogeographic signatures of autotrophic communities.

The discharge of hydrothermal vents on the seafloor provides energy sources for dynamic and productive ecosystems, which are supported by chemosynthetic microbial populations. These populations use the energy gained by oxidizing the reduced chemicals contained within the vent fluids to fix carbon and support multiple trophic levels. Hydrothermal discharge is ephemeral and chemical composition of such fluids varies over space and time, which can result in geographically distinct microbial communities. To investigate the foundational members of the community, microbial growth chambers were placed within the hydrothermal discharge at Axial Seamount (Juan de Fuca Ridge), Magic Mountain Seamount (Explorer Ridge), and Kama'ehuakanaloa Seamount (Hawai'i hotspot). Campylobacteria were identified within the nascent communities, but different amplicon sequence variants were present at Axial and Kama'ehuakanaloa Seamounts, indicating that geography in addition to the composition of the vent effluent influences microbial community development. Across these vent locations, dissolved iron concentration was the strongest driver of community structure. These results provide insights into nascent microbial community structure and shed light on the development of diverse lithotrophic communities at hydrothermal vents.

Abyssal hydrothermal springs-Cryptic incubators for brooding octopus.

Does warmth from hydrothermal springs play a vital role in the biology and ecology of abyssal animals? Deep off central California, thousands of octopus (Muusoctopus robustus) migrate through cold dark waters to hydrothermal springs near an extinct volcano to mate, nest, and die, forming the largest known aggregation of octopus on Earth. Warmth from the springs plays a key role by raising metabolic rates, speeding embryonic development, and presumably increasing reproductive success; we show that brood times for females are ~1.8 years, far faster than expected for abyssal octopods. Using a high-resolution subsea mapping system, we created landscape-scale maps and image mosaics that reveal 6000 octopus in a 2.5-ha area. Because octopuses die after reproducing, hydrothermal springs indirectly provide a food supplement to the local energy budget. Although localized deep-sea heat sources may be essential to octopuses and other warm-tolerant species, most of these unique and often cryptic habitats remain undiscovered and unexplored.

Fluctuation in deep groundwater chemistry and microbial community and their impact on corrosion of stainless-steels.

Low and intermediate level radioactive waste produced during the operation and decommissioning of nuclear power plants is disposed of in an underground geological repository. The majority of metallic waste is made of various stainless-steels and carbon steel. Microbial communities and groundwater composition in deep bedrock at repository sites were believed to stay stable over time, allowing the prediction of evolution of the repository environment. However, a two-year survey of chemical components and microbial community composition within deep bedrock revealed changes in both. An in situ corrosion monitoring system was developed to monitor real-time corrosion rates of two stainless-steel grades (AISI 304 and 316) to study the evolution of corrosion, and correlation between environmental changes and corrosion rate. Surprisingly, higher corrosion rates of steel coupons were detected in the higher alloyed stainless-steel grade 316 compared to the lower alloyed grade 304. Pitting was the main corrosion form. Sulphate reducing bacteria and methanogenic archaea were enriched on surfaces of both types of steel coupons. These microbes likely have a role in the corrosion of stainless-steel in this environment. The changes in groundwater conditions and microbial communities within deep bedrock groundwater at this repository site may have implications for the nuclide release and transport of radioactive material and the long-term evolution and safety of this repository and continental repositories in general and thus needs to be thoroughly understood.

Author Correction: A distinct and active bacterial community in cold oxygenated fluids circulating beneath the western flank of the Mid-Atlantic ridge.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Mariana serpentinite mud volcanism exhumes subducted seamount materials: implications for the origin of life.

The subduction of seamounts and ridge features at convergent plate boundaries plays an important role in the deformation of the overriding plate and influences geochemical cycling and associated biological processes. Active serpentinization of forearc mantle and serpentinite mud volcanism on the Mariana forearc (between the trench and active volcanic arc) provides windows on subduction processes.  Here, we present (1) the first observation of an extensive exposure of an undeformed Cretaceous seamount currently being subducted at the Mariana Trench inner slope; (2) vertical deformation of the forearc region related to subduction of Pacific Plate seamounts and thickened crust; (3) recovered Ocean Drilling Program and International Ocean Discovery Program cores of serpentinite mudflows that confirm exhumation of various Pacific Plate lithologies, including subducted reef limestone; (4) petrologic, geochemical and paleontological data from the cores that show that Pacific Plate seamount exhumation covers greater spatial and temporal extents; (5) the inference that microbial communities associated with serpentinite mud volcanism may also be exhumed from the subducted plate seafloor and/or seamounts; and (6) the implications for effects of these processes with regard to evolution of life. This article is part of a discussion meeting issue 'Serpentine in the Earth system'.

New isotope constraints on the Mg oceanic budget point to cryptic modern dolomite formation.

The oceanic magnesium budget is important to our understanding of Earth's carbon cycle, because similar processes control both (e.g., weathering, volcanism, and carbonate precipitation). However, dolomite sedimentation and low-temperature hydrothermal circulation remain enigmatic oceanic Mg sinks. In recent years, magnesium isotopes (δ26Mg) have provided new constraints on the Mg cycle, but the lack of data for the low-temperature hydrothermal isotope fractionation has hindered this approach. Here we present new δ26Mg data for low-temperature hydrothermal fluids, demonstrating preferential 26Mg incorporation into the oceanic crust, on average by εsolid-fluid ≈ 1.6‰. These new data, along with the constant seawater δ26Mg over the past ~20 Myr, require a significant dolomitic sink (estimated to be 1.5-2.9 Tmol yr-1; 40-60% of the oceanic Mg outputs). This estimate argues strongly against the conventional view that dolomite formation has been negligible in the Neogene and points to the existence of significant hidden dolomite formation.

Ecology of Subseafloor Crustal Biofilms.

The crustal subseafloor is the least explored and largest biome on Earth. Interrogating crustal life is difficult due to habitat inaccessibility, low-biomass and contamination challenges. Subseafloor observatories have facilitated the study of planktonic life in crustal aquifers, however, studies of life in crust-attached biofilms are rare. Here, we investigate biofilms grown on various minerals at different temperatures over 1-6 years at subseafloor observatories in the Eastern Pacific. To mitigate potential sequence contamination, we developed a new bioinformatics tool - TaxonSluice. We explore ecological factors driving community structure and potential function of biofilms by comparing our sequence data to previous amplicon and metagenomic surveys of this habitat. We reveal that biofilm community structure is driven by temperature rather than minerology, and that rare planktonic lineages colonize the crustal biofilms. Based on 16S rRNA gene overlap, we partition metagenome assembled genomes into planktonic and biofilm fractions and suggest that there are functional differences between these community types, emphasizing the need to separately examine each to accurately describe subseafloor microbe-rock-fluid processes. Lastly, we report that some rare lineages present in our warm and anoxic study site are also found in cold and oxic crustal fluids in the Mid-Atlantic Ridge, suggesting global crustal biogeography patterns.

A distinct and active bacterial community in cold oxygenated fluids circulating beneath the western flank of the Mid-Atlantic ridge.

The rock-hosted, oceanic crustal aquifer is one of the largest ecosystems on Earth, yet little is known about its indigenous microorganisms. Here we provide the first phylogenetic and functional description of an active microbial community residing in the cold oxic crustal aquifer. Using subseafloor observatories, we recovered crustal fluids and found that the geochemical composition is similar to bottom seawater, as are cell abundances. However, based on relative abundances and functional potential of key bacterial groups, the crustal fluid microbial community is heterogeneous and markedly distinct from seawater. Potential rates of autotrophy and heterotrophy in the crust exceeded those of seawater, especially at elevated temperatures (25 °C) and deeper in the crust. Together, these results reveal an active, distinct, and diverse bacterial community engaged in both heterotrophy and autotrophy in the oxygenated crustal aquifer, providing key insight into the role of microbial communities in the ubiquitous cold dark subseafloor biosphere.

Oxygen consumption rates in subseafloor basaltic crust derived from a reaction transport model.

Oceanic crust is the largest potential habitat for life on Earth and may contain a significant fraction of Earth's total microbial biomass; yet, empirical analysis of reaction rates in basaltic crust is lacking. Here we report the first assessment of oxygen consumption in young (~8 Ma) and cool (<25 °C) basaltic crust, which we calculate from modelling dissolved oxygen and strontium pore water gradients in basal sediments collected during Integrated Ocean Drilling Program Expedition 336 to 'North Pond' on the western flank of the Mid-Atlantic Ridge. Dissolved oxygen is completely consumed within the upper to middle section of the sediment column, with an increase in concentration towards the sediment-basement interface, indicating an upward supply from oxic fluids circulating within the crust. A parametric reaction transport model of oxygen behaviour in upper basement suggests oxygen consumption rates of 1 nmol cm(-3)ROCK d(-1) or less in young and cool basaltic crust.

The deep subsurface biosphere in igneous ocean crust: frontier habitats for microbiological exploration.

We discuss ridge flank environments in the ocean crust as habitats for subseafloor microbial life. Oceanic ridge flanks, areas far from the magmatic and tectonic influence of seafloor spreading, comprise one of the largest and least explored microbial habitats on the planet. We describe the nature of selected ridge flank crustal environments, and present a framework for delineating a continuum of conditions and processes that are likely to be important for defining subseafloor microbial "provinces." The basis for this framework is three governing conditions that help to determine the nature of subseafloor biomes: crustal age, extent of fluid flow, and thermal state. We present a brief overview of subseafloor conditions, within the context of these three characteristics, for five field sites where microbial studies have been done, are underway, or have been proposed. Technical challenges remain and likely will limit progress in studies of microbial ridge flank ecosystems, which is why it is vital to select and design future studies so as to leverage as much general understanding as possible from work focused at a small number of sites. A characterization framework such that as presented in this paper, perhaps including alternative or additional physical or chemical characteristics, is essential for achieving the greatest benefit from multidisciplinary microbial investigations of oceanic ridge flanks.

Under the sea: microbial life in volcanic oceanic crust.

Exploration of the microbiology in igneous, 'hard rock' oceanic crust represents a major scientific frontier. The igneous crust harbours the largest aquifer system on Earth, most of which is hydrologically active, resulting in a substantial exchange of fluids, chemicals and microorganisms between oceanic basins and crustal reservoirs. Study of the deep-subsurface biosphere in the igneous crust is technically challenging. However, technologies have improved over the past decade, providing exciting new opportunities for the study of deep-seated marine life, including in situ and cross-disciplinary experimentation in microbiology, geochemistry and hydrogeology. In this Progress article, we describe the recent advances, available technology and remaining challenges in the study of the marine intraterrestrial microbial life that is harboured in igneous oceanic crust.

Colonization of subsurface microbial observatories deployed in young ocean crust.

Oceanic crust comprises the largest hydrogeologic reservoir on Earth, containing fluids in thermodynamic disequilibrium with the basaltic crust. Little is known about microbial ecosystems that inhabit this vast realm and exploit chemically favorable conditions for metabolic activities. Crustal samples recovered from ocean drilling operations are often compromised for microbiological assays, hampering efforts to resolve the extent and functioning of a subsurface biosphere. We report results from the first in situ experimental observatory systems that have been used to study subseafloor life. Experiments deployed for 4 years in young (3.5 Ma) basaltic crust on the eastern flank of the Juan de Fuca Ridge record a dynamic, post-drilling response of crustal microbial ecosystems to changing physical and chemical conditions. Twisted stalks exhibiting a biogenic iron oxyhydroxide signature coated the surface of mineral substrates in the observatories; these are biosignatures indicating colonization by iron oxidizing bacteria during an initial phase of cool, oxic, iron-rich conditions following observatory installation. Following thermal and chemical recovery to warmer, reducing conditions, the in situ microbial structure in the observatory shifted, becoming representative of natural conditions in regional crustal fluids. Firmicutes, metabolic potential of which is unknown but may involve N or S cycling, dominated the post-rebound bacterial community. The archaeal community exhibited an extremely low diversity. Our experiment documented in situ conditions within a natural hydrological system that can pervade over millennia, exemplifying the power of observatory experiments for exploring the subsurface basaltic biosphere, the largest but most poorly understood biotope on Earth.