Advances in the microbial mineralization of seafloor hydrothermal systems

L Zhang , Zhi-li Sun Wi Gng *, Hong Cao Yi-hao Qin, Cui-ling Xu Xian-rong Zhang Xin Li , Xi-lin Zhang Hui-ling Song

a Key Laboratory of Gas Hydrate (Ministry of Natural Resources), Qingdao Institute of Marine Geology, China Geological Survey, Ministry of Natural Resources, Qingdao 266071, China

b Evaluation and Detection Technology Laboratory for Marine Mineral Resources, National Laboratory for Marine Science and Technology, Qingdao 266071, China

c China University of Petroleum, Qingdao 266580, China

d Linyi University, Linyi 276000, China

e China University of Geosciences (Beijing), Beijing 100083, China

f Geology Research Institute, Greatwall Drilling Company, Panjin 124010, China

Keywords:

Seafloor hydrothermal systems

Biomineralization

Chemolithoautotrophic microorganisms

Life evolution

A B S T R A C T

Research on the biomineralization in modern seafloor hydrothermal systems is conducive to unveiling the mysteries of the early Earth’s history, life evolution, subsurface biosphere and microbes in outer space.The hydrothermal biomineralization has become a focus of geo-biological research in the last decade,since the introduction of the microelectronic technology and molecular biology technology.Microorganisms play a critical role in the formations of oxide/hydroxides (e.g. Fe, Mn, S and Si oxide/hydroxides) and silicates on the seafloor hydrothermal systems globally. Furthermore, the biomineralization of modern chemolithoautotrophic microorganisms is regarded as a nexus between the geosphere and the biosphere, and as an essential complement of bioscience and geology. In this paper, we summarize the research progress of hydrothermal biomineralization, including the biogenic minerals, the microbial biodiversity, and also the interactions between minerals and microorganisms. In the foreseeable future, the research on hydrothermal biomineralization will inspire the development of geosciences and biosciences and thus enrich our knowledge of the Earth’s history, life evolution and even astrobiology.

1. Introduction

Deep-sea sediments and hydrothermal vent systems have wide ranging gradients of organic matter contents, redox potential, pressure and temperature, which provide habitats for a large number of extreme microorganisms (Yayanos AA,1995; Deming JW, 1998; Vetriani C et al., 1999; Jørgensen BB and Boetitus A et al., 2007). Since the existence of hydrothermal communities were first discovered on the deepsea hydrothermal vents in the Galapagos Rift Valley in 1977,subsequent studies had shown that life on Earth may originate from submarine hydrothermal vent systems (Baross JA and Hoffman SE, 1985; Corliss JB et al., 1979; Martin W et al.,2008), which were of further interest to scientists who had given more attention to microorganisms in hydrothermal vent systems, especially its mineralization, termed as biomineralization. Two years later, the first high-temperature(380±30°C) vent fluids were found at 21° N on the East Pacific Rise (EPR) with fluid compositions remarkably close to those predicted from the lower temperature Galapagos findings. Only here do many species escape from the seafloor in high abundance. Although it was widely believed that only at high temperature hydrothermal vents can many elements,especially metal elements, be discharged from the seafloor at high abundance (Rouxel O et al., 2018), more and more evidence are showing that trace metals such as Fe, Cu and Zn,imported into the ocean have been greatly increased through low-temperature hydrothermal vents which have higher biological activities.

The chemoautotrophic microorganisms, which are the primary energy producers of life metabolism among the abundant kinds of microbes embracing the hydrothermal vent systems, are the basis for the survival and reproduction of hydrothermal communities (Jørgensen BB and Boetitus A,2007; Rouxel O et al., 2018; Elderfield H and Schultz A,1996; Corliss JB et al., 1981). Microorganisms in this system may react with the ambient mineralizing ions actively within seawater because of a series of active sites appearing frequently on their surface (Cox JS et al., 1999; Martinez RE et al., 2002; Yee N et al., 2004), making the biomineralization possible at hydrothermal vents. A large number of studies have also proved that microorganisms play a predominant role in the formations of most minerals in this system. Recently,biomineralization in hydrothermal vents reached a new milestone with the applications of a series of advanced analytic technologies or methods. For instance, Fe isotopic compositions, in associated with nano SIMS (secondary ion mass spectroscopy) and FISH (fluorescenceinsituhybridization), have been applied to study the formation mechanisms and preservation of hydrothermal mineralized microbial mats at Loihi Seamount (Rouxel O et al., 2018;Dauphas N et al., 2017). Here we summarize the mineralization processes of Fe, Mn oxide/hydroxide, silicate,amorphous Opal and S, including the oxidation of H2S and the alteration of metal sulfides (Cao H et al., 2018), through the studies of biomineralization in modern hydrothermal vents. Certain mechanisms and models of biomineralization in seafloor hydrothermal vents are also discussed in order to deepen the understanding and to attract more attention to it.

2. Impact of microorganisms on Fe oxide/hydroxide precipitations

The biomineralization of Fe is probably the most common and important process as far as modern hydrothermal vent systems. Firstly, the content of Fe in the crust ranks fourth(Fortin D and Langley S, 2005). The conversion of valence state between Fe(II) and Fe(III) in redox reaction plays a vital role in the biogeochemical processes of modern environments. Secondly, the biomineralization of Fe may also be an important biochemical process in the early evolution of the Earth, making microbial metabolism dominating the redox reactions of Fe in the overwhelming majority of environments(Weber KA et al., 2006). There are a large number of Fe oxide/hydroxide precipitants characterized by complicated filamentous structures in modern hydrothermal vents, which are quite similar to the morphologies of some neutrophilic Feoxidizing microorganisms themselves or their affiliated structures includingGallionella ferrugineaandLeptothrix discophora(Fortin D and Langley S, 2005; Alt JC, 1988;Juniper SK and Fouquet Y, 1988; Emerson D and Moyer CL,2002; Emerson D, et al., 2007; Kennedy CB et al., 2003;Langley S et al., 2009; Chan CS et al., 2010), revealing that neutrophilic Fe-oxidizing bacteria may impact on the formation of these Fe oxide precipitants significantly.However, since the modern microorganisms obtained from hydrothermal vents are difficult to culture in the laboratory and a part of microorganisms may precipitate Fe on the surface of cells in non-contact ways, the mechanism of Fe precipitate still remains unclear (Forget NL et al., 2010).

Chemoautotrophic Fe-oxidizing bacteria can make CO2fixed by obtaining energy from the oxidation of Fe2+to Fe3+(Sun ZL et al., 2012), which is the most likely cause of Fe oxide precipitation (Kennedy CB et al., 2003; Emerson D,2000). The oxidation rates of Fe with the participation of Feoxidizing bacteria under neutral conditions can be up to four orders of magnitude of inorganic oxidation rate under the same conditions (Kasama T and Murakami T, 2001),indicating the significance of bacteria in the geochemical cycle of Fe. Submarine hydrothermal vents release large amounts of metal-rich high-temperature fluids into the deep sea (Sander SG and Koschinsky A, 2011). In the pure inorganic metal form system, iron is mainly exported in the form of sulfide minerals and oxide particles, only a very small amount of dissolved metal does not precipitate. Strong organic ligands from hydrothermal and seawater sources that bind iron allow large amounts of dissolved metals to flow into the ocean, leaving more available sulfides for the hydrothermal biosphere (Bennett SA et al., 2008; Wu J et al.,2011). Most of these organic ligands are produced by microorganisms (Sander SG and Koschinsky A, 2011). The surface of these microorganisms have many functional groups, such as carboxyl group and phosphate group, which can effectively adsorb positively charged cations, such as soluble Fe and Mn in fluids, enabling some minerals to aggregate and nucleate heterogeneously on the surface of microorganisms (Ueshima M and Tazaki K, 2001). And then,minerals in the fluids begin to precipitate based on these nucleuses. Several other SEM images of samples from the Galapagos Island (Lubetkin M et al., 2018; Fig. 1a), Lau Basin (Sun ZL et al., 2013; Fig. 1b), Troll Wall mounds of Jan Mayen Vent Fields (Johannessen KC et al., 2017; Fig. 1c)and Southwest Indian Ridge (SWIR; Sun ZL et al., 2015; Fig.1d) have shown filament structures that resemble morphologies of Fe-oxides, nontronite, and possible associated microbial remnants.

Fig. 1. Twisted Fe-oxides filament structures with propagating oblate microspheres stemming off of the filaments from the Galapagos islands(a, Lubetkin M et al., 2018), the Lau Basin (b, Sun ZL et al., 2013), the Troll Wall mounds of Jan Mayen Vent Fields (c, Johannessen KC et al.,2017) and the SWIR (d, Sun ZL et al., 2015).

Another reason why the Fe redox microorganisms in hydrothermal vents are so attractive is that we can rebuild the whole process and evolution history of Fe biological cycle by finding reliable biological markers. It was recently proposed that some specific forms of Fe oxides/hydroxides in hydrothermal vents, e.g. long straight rod-like Fe oxides representing the sheath ofLeptothrix discophoraand spiral winding form representing the stalk ofMariprofundus ferrooxydan, can only be produced by the microbial metabolism or by its own mineralization (Sun ZL et al.,2012). The oldest Fe oxide filaments, which were encapsulated in ancient Jasper deposits 170 Ma ago (Sander SG and Koschinsky A, 2011), share extreme similarities with characteristics of theMariprofundus ferrooxydanstrain separated from modern hydrothermal vent systems, which traces life activities of Fe-oxidizing bacteria back 170 Ma.Simultaneously, progresses in relations between some minerals and life activity have been made recently that discuss their significances during biogeochemical cycling as well.Ferrihydrite with two uplift peaks that centered atd=1.5Å andd=2.5Å respectively on the X-ray diffraction (XRD), termed as two-line-ferrihydrite, has the most intimate link with the metabolic activities of neutrophilic Fe-oxidizing bacteria.Their mineral particles are very small (ca. 3 nm; Zhao J,1994) and have a large specific surface area reaching to 100-700 m2/g (Cornell RM and Schwertmann U, 1997),resulting in their strong capacity for adsorption (Zhao J,1994). What’s more, as productions of microbes, ligands which possess functional groups that include carboxylic acids,amines, thiol and hydroxy groups have very high stability constants binding with Fe, making the relative importance of hydrothermal activity for ocean metal budgets revised compared with other trace-metal inputs such as riverine and aeolian sources (Sun ZL et al., 2013). Phosphorus, U, V, Gr and other elements existing in hydrated anions form in the water can be effectively cleaned up by the slightly positive surface of water in hydrothermal systems, which suggest the final metabolic products of Fe-oxidizing microorganisms, as an important sink of trace elements in the ocean, control the geochemical cycle of Fe elements while profoundly affect the geochemical behavior of a series of other elements during the whole ocean cycling (German CR and von Damn KL, 2003).The textural and architectural traits of low-temperature hydrothermal Fe-deposits may not only reflect changes in Feoxidizing microbial populations and minor variations in redox conditions, but could record larger-scale hydrothermal fluctuations, according to recent research (Johannessen KC et al., 2017).

At present, one focus of research on the precipitation of Fe in hydrothermal vent systems is how to quantitatively identify the role of inorganic and microbial factors they play in this process. Although a large number of mineralogical and molecular biology studies have firmly demonstrated the important role of microorganisms in this process, the significance of inorganic factors in such process still cannot be ignored. Not only because of the rapid rate of reductive Fe oxidation in marine environment affected by inorganic processes, but the diagenetic alteration or phase transformation after Fe oxide precipitation also makes the metabolic information of microorganisms obscure, more accuratein situexperiments near hydrothermal vents need to be conducted in the future. Moreover, were there any older Fe-oxidizing bacteria existing during the great oxidation event(GOE) that happened about 2.3-2.4 Ga ago (Bekker A et al.,2004)? How did the cycle of iron in the environment affect their metabolic activity? These problems also need to be figured out in more detailed research on finding ideal biomarkers in modern hydrothermal vents.

3. Impacts of microorganisms on Mn oxide precipitations

Although the content of Mn in basalt is relatively lower(less than 0.2%) compared with Fe, it remains an important energy source without photosynthesis in dark food chain on the seafloor. Compared with moderate to alkaline oxidative seawater, hydrothermal vent systems can provide abundant reductive Mn2+and maintain low dissolved carbon contents,which are ideal environments for autotrophic or facultative Mn-oxidizing bacteria to survive. Recently, a great number of microbial films encapsulated by Fe and Mn oxides have extremely exceeded the capacity of basalt supply obtained on the surface of fresh basalts without obvious weathering occurring at the active volcanoes offshore Hawaii, indicating that the energy of these Fe and Mn-oxidizing microorganisms mostly comes from hydrothermal vent systems (Templeton AS et al., 2009).

Mn-oxidizing bacteria in the hydrothermal environments can increase the oxidation rate of manganese greatly, up to five orders of magnitude or more (Hastings D and Emerson S,1986; Nealson K et al., 1988; Tebo BM et al., 2004);meanwhile, some Mn-oxidizing microorganisms can produce carrier cells to transport Mn(III) (Connell L et al., 2009),giving impacts on mineralization in a deep-sea hydrothermal environment equivalent to Fe-oxidizing microorganisms.Many microorganisms which grow up by using reductive Mn as electron donors, including Mn-oxidizing bacteria or fungi(Templeton AS et al., 2005; Juniper SK et al., 1995; Connell L et al., 2009; Dick GJ et al., 2009), have been found in plumes, in sediments or altered basalts associated with hydrothermal vents. Some Mn-oxidizing bacteria were also separated and cultured from these environments (Templeton AS et al., 2005; Dick GJ et al., 2006; Dick GJ et al., 2009;Ehrlich HL, 1990), such as theBacillusstrain, which is a massive sporulation producer separated by Dick GJ et al.(2009) from plumes and sediments near hydrothermal vents in the Guaymas Basin. The 16S rRNA and mnxG polycopper oxidase coding genes indicate that they were involved in the oxidation of Mn. A common marine bacteriumRoseobacteralso shows the ability to oxidize Mn(II) via its production of extracellular superoxide (Fig. 2). Several studies also indicate that some fungi can form crusts of Mn oxides outside their cells like bacteria, such as theRhodotorula graminisstrain which can gather Mn oxides outside its cell, deepening the recognition of the biomineralization mechanism of Mn in hydrothermal systems (Connell L et al., 2009). As far as we know, more than 30 kinds of Mn oxides/hydroxides have been found (Learman DR et al., 2011). However, the most common ones associated with microbial activities are vernadite (δ-MnO2), birnessite, and todorokite (Tebo BM et al., 2004). For example, in the Guaymas Basin, microbial-derived Mn oxides have been obtained from plumes near hydrothermal vents(Dick GJ et al., 2009), which mainly have the structure ofδ-MnO2or birnessite. They are commonly characterized by poor crystallinity (Villalobos M et al., 2003; Webb SM et al.,2005;), small particle size (only 4-100 nm) (Nelson YM et al.,1999; Kim HS et al., 2004) and aggregate form attached on the surface of cells, which also results in a larger surface area in the range of 98-224 m2/g (Webb SM et al., 2005; Kim HS et al., 2004). Meanwhile, the ordinarily presence of Mn(III)on the surface of Mn(IV) oxides associated with Mn(II) and the holes within octahedral sheets and lattice structures leads to a negative surface for the newly formed Mn oxides in the environment (Tebo BM et al., 2004). This negative surface then absorbs protons and the cations of alkali metals, alkaline earth metals and transition metals effectively, and thus dominate other elements in the surrounding water, such as transition metals, which makes the biomineralization of Mn in hydrothermal systems significant.

Fig. 2. Mn oxides formed in the extracellular superoxide filtrate produced by Roseobacter after 96 h of oxidation (after Learman DR et al.,2011). a-the reacted filtrate within 125 mL erlenmeyer flasks, illustrating the absence and presence of visible Mn oxide particles in the 96 h filtrate. b, c-The subfigures circled by red and yellow frameworks are TEM images of the minerals, respectively, illustrating the presence of dispersed, individual Mn oxides particles after 96 h of oxidation.

4. Biomineralization of silicate minerals and silica in hydrothermal systems

4.1. Biomineralization of silicate minerals

The interaction between microorganisms and silicates including layered silicate and ctosilicate have recently attracted increasing interest. Previous studies have shown that the most common silicate minerals associated with microbial activity in hydrothermal vent systems are nontronite.Nontronite was found partially or completely encapsulated on the cell surface in the Iheya Basin, the Okinawa Trough(Ueshima M and Tazaki K, 2001), the Southern Explorer Ridge (Fortin D et al., 1998), the Eolo Seamount (Dekov VM et al., 2007, 2009), the Galapagos Rift, as well as hydrothermal vent sediments and low-temperature diffusion flow contacted with the mineral surface of the Mariana Trench (Köhler B et al., 1994). These nontronite are characterized by a proper formation temperature of 20-67.3°C for microorganisms to live (Table 1). Besides, most of the nontronite have a filamentous morphology similar to microorganisms and inner circular or elliptical holes in the range of 2-6 μm in diameter, which is probably the residual mold structure after the decomposition of microorganisms.Recently, the remotely operated vehicle (ROV) exploration of the Mashi seamount in the Galapagos Islands discovered an unusual tubular hydrothermal deposit near the summit at 1227 m water depth (Lubetkin M et al., 2018). The porous and friable tubes therein exhibit a strong zonation in color and mineral phases with an interior dominated by bright green nontronite grading outwards to mixtures of nontronite, Fe-Si oxhydroxides, protoferrihydrite, and ending with a more indurated Mn-oxide crust topped with yellowish microbial flock (Fig. 3). Nontronite, an Fe-rich smectite, is the most common clay mineral found on seafloor hydrothermal systems (Sun ZL et al., 2012). It is proposed that the precipitation of Fe-rich nontronite in extracellular polymeric substances (EPS) is due to the concentration and bonding of soluble Si and Fe in fluids by active functional groups such as carboxyl and phosphate groups (Ueshima M and Tazaki K,2001). Its formation may involve complex bonding mechanisms. Metal ions such as Fe, however, can bond the active sites in cell walls with silicate anions through ion bridges, which nucleate minerals on the cell surface first(Fortin D et al., 1998), leading to the formation of filamentous silicate crystals encapsulated on the cell surface.

Table 1. Occurrences of biogenic silicates in modern submarine hydrothermal vent systems.

Fig. 3. The pattern of the tubular hydrothermal deposits captured by ROV near the summit of Mashi Seamount at a depth of 1227 m (Fig.3a). Tube-like hydrothermal deposits near the summit of the Mashi Seamount. Tube diameter in the center of the image is about 20 cm(Fig. 3b; after Lubetkin M et al., 2018). Yellow microbial mat is present in center of the image.

Furthermore, microbial silicate minerals related to modern hydrothermal activities also involve other minerals including zeolite, saponite and some green clays (such as celadonite and glauconite). In addition to the cell wall as a nucleation point,other mechanisms may bond metallogenic substances on cell surface directly and promote mineralization according to the current research. For example, Ivarsson M et al. (2008) found that microorganisms can grow on zeolite as a substrate and form a characteristic biofilm on the surface of zeolite to capture nutrients in the fluid for their own survival whereas Geptner A et al. (2002) suggested that the formation of saponite in a hydrothermal system may be a phase transformation or recrystallization of a gelatinous substrate under the catalysis of microorganisms. Moreover, Tazaki K and Fyfe WS (1992) showed that green clay, which includes glauconite and celadonite, was formed by the alteration of volcanic debris catalyzed by microorganisms in hydrothermal environment, which was confirmed by accompanying graphitized microbial residues. Similar phenomena have also been found in modern hot springs exposed on the ground(Konhauser KO et al., 2002). All the above studies undoubtedly show that the microbial mineralization of silicates, especially clay minerals, is ubiquitous, though the formation of silicate minerals in modern hydrothermal vents has not received sufficient attention. This should be an important area for further research in the future.

4.2. Precipitation of silica microbial mineralization and growth mode of Si-rich chimney

The most recent research on microbial silicification focuses on hot springs exposed on land surfaces, among which the most widely studied areas include Yellowstone National Park (Guidry SA and Chafetz HS, 2003), Iceland(Konhauser KO et al., 2001), and New Zealand (Jones B et al., 2007). In fact, hydrothermal fluids above the modern seafloor are also Si-rich, resulting in the widespread occurrence of filament resembling microorganisms, which are mainly composed of amorphous opal (Opal-A) in modern submarine hydrothermal vents (Stüben D et al., 1994; Al-Hanbali HS et al., 2001), consisting of the important part of modern hydrothermal deposits associated with sulfides and Fe-Mn oxides. Growth models of the low-temperature hydrothermal Fe- and Si-rich chimney from the CDE hydrothermal field have been reported recently (Sun ZL et al.,2012; Fig. 4). Moreover, the process of silicification among several hydrothermal microorganisms in Si-rich fluids has been simulated in the laboratory (Orange F et al., 2009). One target they want to achieve is to figure out the role microorganisms played in the process of silicification,because arguments remain whether microorganisms are passively used as precipitation templates or actively induce silica to mineralize on their own surfaces and thus obtain energy from them. Another target is to understand the evolution of the ancient Earth, especially the Precambrian. It has gradually been agreed that the formation environment of oxygen-deficient, relatively high temperatures and reductive fluids in the modern mid-ocean ridge system, is similar to the surface of the early Earth (Orange F et al., 2009), and the morphology of silicified microorganisms found in Archean sediments is very similar to that of modern microorganisms(Westall F et al., 2006). The study of the microbial silicification mechanism in modern hydrothermal environments can promote research on various geological phenomena such as the banded iron formation (BIF) in Ferich and Si-rich oxides, hydrothermal activities, and the course of life evolution during the early Earth. Modern hydrothermal Fe-Si oxyhydroxide deposits are now known to be analogues to ancient siliceous iron formations (Sun ZL et al., 2015; Fitzsimmons JN et al., 2017; Lough AJM, et al.,2017). The authors believe that the development of research,and the future research on microbial silicification in hydrothermal environment needs to transfer from land to sea.By means of combiningin situexperiments with laboratory simulations, comparing the ancient and modern mechanisms of silicification in hydrothermal microbial mineralization could activate the research on Si deposit both on land and in the ocean.

Fig. 4. Growth model of the low-temperature hydrothermal Si-rich chimney from the CDE hydrothermal field (modified from Sun ZL et al.,2012). a-Owing to the suitability of fluid temperature and supplement of abundant nutrient substances, neutrophilic Fe-oxidizing bacteria pervasively exist in the interior of the mineral ring and result in the abundant precipitation of the Fe-rich oxide, which gradually forms a main body of this layer. The fluid temperature is supposed to range from 10-30°C; b-the increasing precipitation of biogenic Fe oxide filaments gradually reduces the permeability of the mineral ring. As a result, the hydrothermal fluid-seawater mixing is restricted and the temperature of the fluids inside the ring is prompted to about 40 °C. The dissolved silica then get to be supersaturated with respect to opal-A and extensive precipitation of silica happens; c-an extensive precipitation of opal-A restricts and retards the hydrothermal fluid-seawater mixing with the temperature of the fluids inside the chimney being elevated to 70-100 °C. Barite and opal-A are precipitated from this fluids and the permeability of the chimney wall decreased sharply. Most of the hydrothermal fluids emitted from the main conduit and the chimney get to the summit in its growth history; d-the chimney wall becomes thicker and denser and the exchange of hydrothermal fluids and seawater ceases. As a result, a Fe-Mn oxide layer precipitates onto the outer surface of the chimney wall as neutrophilic Fe-oxidizing bacteria reoccupy the surface of the chimney once again. Ultimately, the main conduit of the chimney is stuffed by continued mineral precipitations and the chimney gets to an extinct state.FC-fluid channel.

5. Biomineralization of sulfide in seafloor hydrothermal systems

Microbial oxidation of various reduced S, especially H2S whose oxidation represents the most important energy source for the microbial community during the mixing of seawater and hydrothermal vent fluids, is the key in C and S biological cycles in hydrothermal vent systems (Sievert SM et al., 2008).The results of extensive studies show the most important sulfur-oxidizing microorganisms in the hydrothermal vent environment exist in symbiotic or free-growing forms,including strains ofGammaproteobacteria,Epsilonproteobacteria, andAquificaceae.

Microbial oxidation of sulfur in hydrothermal environment leads to the formation of various minerals, such as S, metal sulfides and sulfates, etc. Filamentous S, for example, is the most common product in the transition environment between H2S and O2, and is also the most important biological process quantitatively in hydrothermal vent environment (Taylor CD et al., 1997; 1999; Rasmussen B, 2000). The phenomenon of white flocculent substances ejection together with submarine fluids is frequently found in the hydrothermal areas where eruptions have just taken place or where large-scale hydrothermal fluids are excreted (Taylor CD, 1999; Nelson D et al., 1991; Embley RW Jr et al., 1995;Embley RW et al., 2000; Moyer CL et al., 1995). These flocculants are composed of inorganic S and mineralized S-oxidizing bacteria (Nelson D et al., 1991), which indicates the universality and importance of S-utilizing microorganisms in hydrothermal vents. The chemical composition and structure of the micro-zone of samples obtained from the hydrothermal fields of the EPR and the Mid-Atlantic Ridge (MAR) had been studied (Foriel J et al., 2004) using particle-induced X-ray fluorescence analysis (PIXE) and micro X-ray absorption near-edge structure (micro-XANES), suggesting that both mineralized and living microbial surfaces have complex sulfur-bearing minerals, including sulfate, sulfite and organic sulfur, showing the complex metallogenic mechanism of S-oxidizing bacteria. Zierenberg RA and Schiffman (1990)found that the catalytic process of some microorganisms selectively precipitated Ag, As and Cu elements first,indicating that microbial catalysis may be an important reason for the enrichment of some precious metals in some submarine hydrothermal metal sulfide deposits.

The energy effect of the oxidation of metal sulfides,compared with the oxidation of H2S, is smaller. But the oxidation of residual metal sulfides may be an important guarantee for the continued existence and reproduction of microorganisms supporting the synthesis of chemical energy(Juniper SK et al., 1988; Eberhard C et al., 1995) under conditions of H2S depletion after the activities of hydrothermal systems. Metal sulfides in hydrothermal systems can provide at least 40% of the energy for the growth of chemosynthetic microorganisms in the system according to McCollom TM (2000). Metal sulfide sulfides are directly oxidized by contact with seawater, showing weathering characteristics such as the corrosion pits on mineral surfaces on microscale (Verati C et al., 1999) and the existence of large orange-brown crust mainly composed of secondary Fe oxides/hydroxides especially on extinguished spires/chimneys(Juniper SK and Tebo BM, 1995) as well as debris accumulation and weathering products (Scott SD, 1997).Wirsen CO et al. (1993) and Eberhard C et al. (1995) both have separated specific sulfur-oxidizing chemoautotrophs,which can oxidize metal sulfides under near-neutral conditions, during the research about the microbial mat on the surface of polymetallic sulphide deposits in the Trans-Atlantic Geotraverse (TAG) and the Snake Pit of the MAR. Eberhard C et al. (1995) carried outin situ, deck and laboratory comprehensive work to study the oxidation process of sulfide by thermophilic aerobic sulfur oxidizing bacteria and both experimental results showed that14CO2fixation occurred during the oxidation process of metal sulfide. Edwards KJ et al. (2003) carried outin situculture experiments of minerals including elemental S and various metal-bearing (Cu, Fe, Pb)sulfides near hydrothermal vents and two months later, the original smooth mineral surface was altered to varying degrees, occupied by various microorganisms and secondary minerals, of which the surface microbial density of S was the largest, demonstrating that S-oxidizing microorganisms and Fe-oxidizing microorganisms both play an important role in the alteration of metal sulfides. These studies have proved that sulfur-oxidizing microorganisms in hydrothermal vent systems can obtain sufficient energy from various forms of sulfides, which provides an important material basis for the existence of deep-sea hydrothermal vent communities.However, more work is needed to support the study of energy provided by sulfides quantitatively and demonstrate the mechanism and significance of microbial metabolisms.

6. Significance and prospects

Hydrothermal vent systems, as the cradle of life, were distributed widely on the surface of the Earth (Santelli CM,2009) 4 Ga ago, breeding unique communities around them.Microbial information in each period can be well preserved(Juniper SK and Fouquet Y, 1988; Juniper SK and Tebo BM,1995; Westall F and Southam G, 2006) because the mineral precipitation in the hydrothermal system has a relatively faster precipitation rate together with the mineralization of various microorganisms commonly involved. Experiments show that whether the original morphology and composition of microorganisms can be effectively preserved through mineralization depends not only on the influence of late diagenesis and weathering alteration, but also on the very short period of time (for example, days to months) during the early stage of mineralization (Orange F et al., 2009),indicating that the study of microbial mineralization in hydrothermal vent area during geological history can provide a series of reliable evidence for the history of the Earth and the evolution of life. For example, mineralized organisms have been identified in deep-sea volcanic massive sulfide(VMS) deposits from the Sulfur Springs, Australia 3.235 Ga ago. Furthermore, silicified coccoid microorganisms have been found in volcanic clastic rocks from Pilbara Craton 3.466 Ga ago, which also significantly promote the study of life evolution history. Studies on modern hydrothermal vents have been revealing the widespread existence of the biosphere beneath the seafloor (Jørgensen BB and Boetius A, 2007;Ivarsson M et al., 2008; Fisk MR et al., 1998). The filamentous microbial fossils commonly found in submarine hydrothermal systems, together with some biogenic minerals,also exist in the biosphere beneath the seafloor (Ivarsson M,2008; Hofmann BA et al., 2008). Recognizing primary,biogenic structures in fossils and the effects of diagenesis is important in the use of fossils in geochemistry, in the understanding of metazoan evolution, and in the reasonable interpretation of how geological events impacted the biosphere (Pérez-Huerta A et al., 2018). The study of microbial mineralization in hydrothermal vent systems is the most important key to understanding the subseafloor deep biosphere. Similarly, the study on mineralization of microorganisms in modern hydrothermal vents is also needed if we want to explore astronomical microorganisms because the surface environment of some terrestrial planets, such as Mars, is very similar to the modern hydrothermal vent system of the Earth (Al-Hanbali HS et al., 2001; Orange F et al.,2009; Hofmann BA et al., 2008; Kyle JE et al., 2007).

With more and more studies on microbial mineralization in seafloor hydrothermal systems reported from all over the world and the introduction of molecular biology as well as the development of microelectronic detection technology, the research on biodiversity and microbial mineralization of hydrothermal vents has been developed in depth, and has gradually become a hot spot in life science and geological microbiology. At present, the study of microbial mineralization in hydrothermal vent systems is still focused on micro-mineralization mechanism and microbial diversity,while the role of microorganisms on a macro-scale in hydrothermal deposit formations and late ore body transformation is seldom involved. Since the isolation and pure culture of microorganisms in extreme environments is difficult, there are still problems in simulating the mineralization process of most hydrothermal microorganisms under laboratory conditions. Some biomarkers indicating specific taxonomic or metabolic processes are still difficult to find (Chan CS et al., 2010). Besides, compared with the mature microbial metallogenic studies of Fe, Mn and S, the microbial metallogenic processes of other elements/minerals,such as Opal-A and silicate minerals in hydrothermal vent system, are still weak. All these problems need further research.

7. Conclusions

Organic-inorganic interactions are pervasive in modern seafloor hydrothermal systems, which also make biomineralization a key area in the life sciences and geomicrobiology research. This paper summarizes the current research status of biomineralization in seafloor hydrothermal environments, and concludes that: (1) neutrophilic Feoxidizing microorganisms have played a key role in the precipitation of reductive hydrothermal Fe, and their mineralized products have the potential as credible biological markers to search for ancient Earth life; (2) manganese is also an important energy source for the so-called “dark food chain” that does not rely photosynthesis in oceans;meanwhile, Mn-oxidizing microorganisms probably give impacts on mineralization in deep-sea hydrothermal systems equivalent to Fe-oxidizing microorganisms; (3) nontronite is a typical product of microbial mineralization in the hydrothermal sediments, but other minerals such as zeolite,saponite, celadonite and glauconite may also be related to the mediation of microorganisms; (4) microbial silicification in hydrothermal systems is very common and may also be an important mechanism for the preservation of ancient microorganisms in old sediments; (5) sulfur-oxidizing microorganisms in hydrothermal habitat can obtain enough energy from various forms of sulfides to provide the most important material basis for the existence of chemosynthetic ecological communities. Although there has been considerable progress in the study of hydrothermal biomineralization, it is still far from sufficient for us to explore the evolution of Earth life and even the urgent needs of extraterrestrial life. Finally, it is recommended that the exploration and corresponding study in hydrothermal biomineralization be further strengthened in the future.

Acknowledgement

This study was supported by the Natural Science Foundation of China (91858208, 41606086, 41606087),National Key Basic Research and Development Program of China 2017YFC0307704) and the Marine Geological Survey Program of China Geological Survey (DD20190819).