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Scientific and technological progress in the microbial exploration of the hadal zone

  • Corresponding author: Weipeng Zhang, zhangweipeng@ouc.edu.cn
  • Received Date: 2020-06-08
    Accepted Date: 2021-05-11
    Published online: 2021-08-10
  • Edited by Chengchao Chen.
  • The hadal zone is the deepest point in the ocean with a depth that exceeds 6000 m. Exploration of the biological communities in hadal zone began in the 1950s (the first wave of hadal exploration) and substantial advances have been made since the turn of the twenty-first century (the second wave of hadal exploration), resulting in a focus on the hadal sphere as a research hotspot because of its unique physical and chemical conditions. A variety of prokaryotes are found in the hadal zone. The mechanisms used by these prokaryotes to manage the high hydrostatic pressures and acquire energy from the environment are of substantial interest. Moreover, the symbioses between microbes and hadal animals have barely been studied. In addition, equipment has been developed that can now mimic hadal environments in the laboratory and allow cultivation of microbes under simulated in situ pressure. This review provides a brief summary of recent progress in the mechanisms by which microbes adapt to high hydrostatic pressures, manage limited energy resources and coexist with animals in the hadal zone, as well as technical developments in the exploration of hadal microbial life.
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Scientific and technological progress in the microbial exploration of the hadal zone

    Corresponding author: Weipeng Zhang, zhangweipeng@ouc.edu.cn
  • 1. College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China
  • 2. State Key Laboratory of Microbial Technology, Shandong University, Qingdao 266237, China
  • 3. Department of Chemistry, The University of Hong Kong, Hong Kong, China

Abstract: The hadal zone is the deepest point in the ocean with a depth that exceeds 6000 m. Exploration of the biological communities in hadal zone began in the 1950s (the first wave of hadal exploration) and substantial advances have been made since the turn of the twenty-first century (the second wave of hadal exploration), resulting in a focus on the hadal sphere as a research hotspot because of its unique physical and chemical conditions. A variety of prokaryotes are found in the hadal zone. The mechanisms used by these prokaryotes to manage the high hydrostatic pressures and acquire energy from the environment are of substantial interest. Moreover, the symbioses between microbes and hadal animals have barely been studied. In addition, equipment has been developed that can now mimic hadal environments in the laboratory and allow cultivation of microbes under simulated in situ pressure. This review provides a brief summary of recent progress in the mechanisms by which microbes adapt to high hydrostatic pressures, manage limited energy resources and coexist with animals in the hadal zone, as well as technical developments in the exploration of hadal microbial life.

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Introduction
  • The hadal zone is known to be the deepest region in the ocean. It was named after Hades, the realm of the underworld in Greek mythology, and arguably remains the least explored and most mysterious environment on Earth. One of the major features of the hadal zone is the trenches, and there are a total of 27 subduction trenches, 13 troughs, and seven trench faults below 6000 m (Jamieson et al. 2009; Stewart and Jamieson 2018). The deepest point of the hadal zone is the Challenger Deep, part of the Mariana Trench, which is 10, 902 to 10, 929 m deep (Fryer et al. 2003). The potential temperature of seawater in the hadal zone is approximately 1.05 ℃, which is slightly higher than that at 6000 m (~ 1.03 ℃) but much lower than the average temperature of the abyssopelagic zone (4000-6000 m) (~ 1.1 ℃) (Gamo and Shitashima 2018). The salinity and dissolved oxygen concentration are approximately 3.47% and 164 µmol/kg, respectively, somewhat higher than those in the abyssopelagic zone (Gamo and Shitashima 2018). The morphology of hadal environments provides a unique organic carbon depositional system that differs from other parts of the deep sea. The axes of the trenches may act as quantitatively important hot spots for the deposition and microbial mineralization of organic material in the deep sea (Wenzhöfer et al. 2016). A high sediment organic matter content and biological activity are apparently sustained by the lateral transport of material from their surroundings and subsequent downslope focusing of labile organic material (Gooday et al. 2010; Ichino et al. 2015; Luo et al. 2017; Turnewitsch et al. 2014). Higher benthic oxygen consumption rates at a depth of 11, 000 m water (Challenger Deep, Mariana Trench) compared with the nearby abyssal zone were discovered by in situ measurements, reflecting intensified diagenetic activity in the trench axis sediments (Glud et al. 2013).

    Despite the challenging physical and chemical conditions, animals are found in the hadal zone, including deep-sea fish and amphipods (Jamieson et al. 2009; Linley et al. 2017). Prokaryotes, such as Proteobacteria and Bacteroidetes, have also been studied (Nunoura et al. 2018). Recent estimates of seawater microbial-cell density in the hadal zone (Arístegui et al. 2009; Peoples et al. 2018) indicate that they are comparable to those in the abyssopelagic zone, i.e., approximately 104 cells/ml. Sediment microbial biomass in the hadal zone was also greater than in abyssal zone sediments, particularly in the deeper layers (Glud et al. 2013; Hiraoka et al. 2020; Nunoura et al. 2015, 2018; Wenzhöfer et al. 2016). For example, at 6000 m the average abundance of prokaryotes was approximately 1.4 × 106 cells/cm3 on the sediments surface, while the abundance in Challenger Deep surface sediments, had a density of up to approximately 9.7 × 106 cells/cm3 (Glud et al. 2013). The prokaryotic abundance in hadal zone sediments of the Izu-Bonin, Tonga and Mariana Trenchs were 7.6 × 108 cells/cm3, 1.2 × 108 cells/cm3, and 1.4 × 108 cells/cm3, respectively (Wenzhöfer et al. 2016). In Challenger Deep (Mariana Trench) sediments the abundance of cells ranged between 6.3 × 105 and 1.5 × 108 cells/ml at a depth of 10, 300 m (Nunoura et al. 2018). Thus, all reports have confirmed that there are abundant microorganisms in hadal zone sediments.

    Studies on the taxonomy of microbes in hadal environments have shown that Gammaproteobacteria are dominant in seawater, while Marine Group Ⅰ (MGI) Thaumarchaeota and Candidatus Woesearchaeota are dominant in sediments (Nunoura et al. 2018). More recently, Hiraoka et al. (2020) found that at several hadal sites geochemical parameters, such as nitrate, total organic carbon and total nitrogen varied along with surface productivity. The relative abundances of Chloroflexi, Woesearchaeota, and Marinimicrobia generally increased in parallel with gradual decreases in oxygen and nitrate concentrations in hadal sediments (Hiraoka et al. 2020). In addition, microbes that cohabit with hadal animals have started to attract the attention of marine biologists (He et al. 2018; Zhang et al. 2019b).

    The underlying mechanisms governing the adaptation of microorganisms to these deep-sea environments are of substantial interest. Considerable advances in technology for the exploration of deep-sea life have been made since the turn of the 21st century, including full-ocean-depth-rated modular landers developed for in situ measurements and renewed high-pressure culture techniques, resulting in the development of hadal microbial communities as a research hotspot. There are several extensive reviews on hadal environment macro-organisms (Bruun 1950; Wang et al. 2020; Xu et al. 2018) but here we focus on microbial adaptation to the hadal zone environment and the technological developments supporting the exploration of microbial life in this unique biosphere.

How microbes cope with high pressure in the hadal zone
  • The environmental adaptations of hadal microbes have been already received some attention (Fig. 1). The cell membrane works as a barrier between microbes and the outside world under high hydrostatic pressures. The microbial membrane can rapidly switch to a gel state from a relatively free-flowing liquid-crystal state (Denich et al. 2003). The gelled membrane can induce membrane protein aggregation and reduce protein activity, which, in turn, leads to the limitation of membrane biological functions by affecting membrane stability and permeability (Jebbar et al. 2015; Lee 2004). Thus, one strategy to combat high pressure is to adjust the state of the cell membrane. Sinensky (1974) modeled basic homeoviscous adaptation and found that some bacteria are able to maintain membrane fluidity under high hydrostatic conditions. Subsequent studies have indicated that three mechanisms are primarily involved. Firstly, microbes can adjust the proportion of unsaturated fatty acids to change the gel state of the membrane. For example, Photobacterium profundum strain SS9 up-regulates the expression of related fatty-acid-synthesis genes under high hydrostatic pressure to increase the proportion of monounsaturated and polyunsaturated fatty acids in the membrane (Allen and Bartlett 2000; Allen et al. 1999). Secondly, microbes can adjust the content of branched fatty acids in the membrane. Desulfovibrio indonesiensis strain P23 changes the proportion of fatty-acid branches when the outside pressure increases (Fichtel et al. 2015; Zhang and Rock 2008). Thirdly, microbes can change the length of acyl chains to maintain membrane fluidity. Increasing the carbon chain length by two atoms increases the phase-transition temperature of the lipid by 10-20 ℃ and reduces the permeability of the membrane to water (Jebbar et al. 2015). With an increase in pressure, Clostridium paradoxum cells tend to shorten the length of branched-chain fatty acids and this shortening occurs for all major types of phospholipid fatty acid (Scoma et al. 2019). Interestingly, the mechanisms adopted by gram-negative bacteria are usually different from those of gram-positive bacteria. While gram-negative bacteria often adjust the proportion of unsaturated fatty acids, gram-positive bacteria tend to adjust the content of branched fatty acids and both gram-negative and gram-positive bacteria change the length of fatty-acid acyl chains (Wang et al. 2014).

    Figure 1.  A schematic model for microbial adaptation to high hydrostatic pressure, carbon source utilization, and animal gut microbial function in the hadal zone. Microbes increase the proportion of unsaturated and branched fatty acids to maintain membrane fluidity under high pressures. Alkanes and polysaccharides recycled in the ocean bottom, which can remain for a long time, are important carbon sources for the hadal microbiota. The gut microbiota of hadal amphipods have lost the genes to reduce trimethylamine N-oxide (TMAO), which results in its accumulation to combat high pressure. In addition, the amphipod gut microbiota can acquire choline, carnitine, and glycine-betaine

    High hydrostatic pressure also inhibits cell division, motility and intracellular enzyme activity, resulting in the cessation of the cell cycle (Yin et al. 2017). Thus, another strategy adopted by microbes to adapt to high hydrostatic pressure is to use osmotic protection agents to maintain the osmotic pressure balance. The well-known osmolyte trimethylamine N-oxide (TMAO) is a small molecule that is widely distributed in marine environments and prevents the adverse effects of osmotic pressure, low temperature, and high hydrostatic pressure (Ge et al. 2011). Mechanistically, TMAO is likely to function as an important stabilizer for protein folding and nucleic acids (Petrov et al. 2012; Ufnal et al. 2015). It protects channel protein structures from high hydrostatic pressure by forming a 'protective shielding layer' around the proteins being folded (Petrov et al. 2012; Ufnal et al. 2015). In the case of piezosensitive bacteria, TMAO promotes the growth of the Vibrio fluvialis strain QY27 by increasing the expression of torA and enzyme activity under high hydrostatic pressures (Yin et al. 2017). Similarly, TMAO reductases are up-regulated under high hydrostatic pressures in the piezophilic bacteria Photobacterium profundum SS9 and P. phosphoreum ANT-2200 (Campanaro et al. 2005; Li et al. 2013; Zhang et al. 2016). Studies on isolates and the use of genomics have confirmed that some microorganisms from the hadal zone can use TMAO to protect themselves from high hydrostatic pressure (Peoples et al. 2020; Zhang et al. 2018a).

    Some hadal zone microorganisms have unique mechanisms for environmental adaptation. The existence of the 'Hadal Biosphere' has been identified in the Challenger Deep of the Mariana Trench. The carbon turnover and oxygen consumption rates of hadal zone microorganisms are higher than those of adjacent deep-sea areas (Nunoura et al. 2016). Compared with their surface ecotypes, the genera Photobacterium, Pyrococcus, and Shewanella from the hadal zone lack many metabolic loci for the degradation of simple organic compounds, while the genes for the degradation of organic polymers were enhanced (Oger and Jebbar 2010). In piezophilic Shewanella, external growth pressure significantly altered the respiratory chain components, leading to the presence of two types of respiratory chains that are regulated in response to pressure (Oger and Jebbar 2010). Hadal bacteria were also found to accumulate protein‐stabilizing solutes, such as the piezolytes β‐hydroxybutyrate and oligomers of β‐hydroxybutyrate (Martin et al. 2002). Archaea present in the Puerto Rico Trench synthesize fatty acids and are able to recover ammonia, carbon dioxide and methyl, indicating new metabolic capabilities (Leon-Zayas et al. 2015). In addition, NhaD-type sodium/proton antiporters and aquaporins for osmotic adjustment were also found in Nitrosopumilus (Leon-Zayas et al. 2015). Wang et al. (2019a) found that Thaumarchaeota can encode A-type or V-type ATPase. The V-ATPase with a proton pump function is present in the deep sea, providing suitable advantages for deep-sea ammonia-oxidizing archaea under high pressure.

How microbes acquire carbon and energy sources in the hadal zone
  • In addition to the high hydrostatic pressure, the organic and inorganic materials in hadal waters also play key roles in influencing microbial lifestyles. Thus, it is important to understand the diversity and metabolism of hadal microorganisms, since these findings could have important consequences for understanding these unique microbial ecosystems and their roles in the biogeochemical cycling. There is evidence to show that heterotrophic groups that utilize complex carbohydrates are widespread in the hadal zone (Peoples et al. 2018). For example, as shown by 16S rRNA gene analyses of microbes in the Mariana Trench, there are major populations of Gammaproteobacteria, including Pseudomonas and Pseudoalteromonas, that show heterotrophic activities (Peoples et al. 2018; Tarn et al. 2016). An abrupt increase in hydrocarbon-degrading bacteria was observed close to the Mariana Trench bottom and the metabolism of these microbes was demonstrated by utilizing n-C16/18 in both culture-dependent and culture-independent methods (Liu et al. 2019b). In particular, Alcanivorax strains that expressing genes involved in alkane degradation were discovered in high abundance (Liu et al. 2019b). In addition, hadal microbial lineages can even metabolize polymers (Lauro and Bartlett 2008; Tian et al. 2018). Several common deep-sea bacteria, including Pseudoalteromonas and Myroide, are potential degraders of large organic polymers. Pseudoalteromonas sp. SM9913 can swim in seawater and gather on the surface of sediment particles to obtain nutrients (Qin et al. 2011; Zhao et al. 2008), while Myroides profundi D25 can digest insoluble collagen (Ran et al. 2014). The complex carbohydrate-degrading Euzebyella marina has also been found in the hadal zone (Liu et al. 2019a). Members of this species use the potential intracellular cycling of the glycogen/starch pathway and glycoside hydrolases that differ from those of other Flavobacteria (Liu et al. 2019a). Furthermore, it was also found that several groups of hadal microbes possess the potential activity to degrade recalcitrant dissolved organic matter. For example, Chloroflexi and SAR202 encoded and expressed alkanal monooxygenase and catechol 2, 3‐dioxygenase genes to oxidize aromatic compounds (Gao et al. 2019). In addition to heterotrophic carbon metabolism, a recent study of the distribution of MGI Thaumarchaeota, which are important players in the ocean biogeochemical cycling of nitrogen and carbon (ammonia oxidizers in the hadal zone), provided evidence that these hadal residents perform ammonia oxidation and carbon fixation (Zhong et al. 2020). Recently, Xue et al. (2020) found that biodiversity in the Mariana Trench increased with depth. The glycolytic pathway is more common in surface water, while in the deepest water area (> 10, 000 m), gluconeogenesis, the glyoxylate shunt, and oxidative phosphorylation are more common ways to reduce the demand for carbon.

    The correlation between carbon utilization and the formation of microbial communities in hadal waters is still not fully understood but several researchers have postulated hypotheses to explain the dynamics of the hadal microbial sphere. For example, Nunoura et al. (2015) inferred that the formation of hadal microbial populations was a result of the endogenous recycling of organic matter associated with trench geomorphology. This hypothesis is consistent with the finding that organic matter can be suspended in the water column by earthquakes (Kawagucci et al. 2012). Because of the narrow shape of trenchs, regular earthquakes may offer a steady supply of sinking and suspended organic particles (Kawagucci et al. 2012). This hypothesis is also supported by the isolation of several alkane-degrading strains from the benthic surface of the Mariana Trench. These bacteria prefer to utilize even-chain over odd-chain alkanes (Liu et al. 2019b). These alkanes are usually generated by photoautotrophs or found in sinking particles (Ekpo et al. 2005; Guan et al. 2019; Mille et al. 2007), suggesting that even-chain alkanes in the hadal surface sediments have a very different source and are likely to be synthesized in situ or released from sediments. Viral communities and their biological impacts have also been studied. Single-stranded DNA (ssDNA) viral families, including Microviridae, Circoviridae, and Geminiviridae, have been demonstrated to be the major groups among viral metagenomes in the hadal sediments (Yoshida et al. 2013). In oceanic sediments between 1000 and 10, 000 m deep, the impact of viral infection is higher on archaea (primarily directed at members of specific clades of MGI Thaumarchaeota) than on bacteria (Danovaro et al. 2003). In addition, lytic bacteriophages are hypothesized to reduce the rates of benthic microbial processes and release organic material by a viral shunt, indicating that bacteriophages have important effects on the substrate biosphere (Kyle et al. 2008; Pedersen 2012). Thus, hadal trenches may be characterized by a highly dynamic viral component, which can profoundly influence the function of these hadal ecosystems (Manea et al. 2019).

How microbes cohabit with hadal animals
  • One important perspective in understanding microbial adaptation is to explain how symbiotic microbes establish mutually beneficial relationships with their hosts. Animal gut microbiota successfully establish such a relationship by making significant contributions to the physiology and health of their hosts. Gut microbial studies have received increasing attention in recent years, as is apparent from the many papers that have been published on the human gut microbiota. In contrast, despite the discovery of a variety of animals in the hadal zone, the gut microbiotas of these mysterious animals has received scant attention.

    Amongst the most abundant animals living in hadal habitats are amphipods of the superfamily Lysianassoidea. The discovery of this animal can be traced to a study in 1959 in which the scavenging amphipod Hirondellea dubia was described (Dahl 1959; Wilson et al. 2018). Amphipods that inhabit the hadal zone play key roles in other deep-ocean ecosystems and the endemism of these species renders them good models for the study of feeding behaviors, evolutionary processes and the restricted distribution of animals in hadal trenches. A popular view is that hadal amphipods rely on necrophagy for food (De Broyer et al. 2004) and thus microbial communities of many taxa can be found in their digestive tracts. Kobayashi et al. (2012) reported the activities of amylase, cellulase, mannanase, xylanase, and α-glycosidase in an extract of the body of the giant amphipod Hirondellea gigas collected from Challenger Deep and found that these enzymes were able to digest plant-derived polysaccharides under a high hydrostatic pressure of 100 MPa at 2 ℃. These results strongly suggest that H. gigas adapted to its extreme oligotrophic hadal oceanic environment by evolving digestive enzymes (Kobayashi et al. 2012). In contrast, through a larger-scale sampling and metagenomic study, Zhang et al. (2018a) reported the existence of tens of microbial species in the gut of the amphipod H. gigas from the Challenger and Sirena Deeps. The guts of the 11 investigated amphipod individuals were dominated by the same bacterial strain, designated Psychromonas sp. CDP1. Genomic analysis suggested there was a substantial reduction of the Psychromonas sp. CDP1 genome compared with that of its closest relatives found in shallower seawater. Deletion of the TMAO-reducing gene cluster has been observed in CDP1. TMAO is versatile at improving pressure tolerance: it can be used as a 'piezolyte' to enhance protein folding and counteract hydrostatic pressure, and it can also improve growth under high pressure through TMAO respiration. The deletion of the TMAO-reducing genes implies that the bacterium and its hosts utilize TMAO to manage the high pressure (Zhang et al. 2018a). Furthermore, CDP1 lacks a variety of carbohydrate-utilization pathways, suggesting that this bacterium is confined to the gut environment and may have established a close relationship with the host in terms of sharing resources (Zhang et al. 2018a). Zhang et al. (2019a) then compared populations of H. gigas from the Mariana and Japan Trenchs with respect to the microbial composition and metabolic features of their gut microbiota, and found that there were significant differences in composition of their gut microbiota between the two trenches. Variation in the abundances of Psychromonas, Propionibacterium, and Pseudoalteromonas species, in particular, was recorded. The proportion of carbohydrate-recycling genes was also significantly higher in the guts of H. gigas individuals from the Mariana Trench, which could be a result of the limited availability of carbon in this trench (Zhang et al. 2019b). Subsequently, Cheng et al. (2019) compared the gut microbial composition of two hadal amphipod species, H. gigas and Halice sp. MT-2017, which were the dominant species in the Challenger Deep. Although the bacterium 'Candidatus Hepatoplasma' was dominant overall, Psychromonas was abundant in H. gigas and Psychrobacter was abundant in Halice sp. MT-2017, suggesting the use of different strategies in recruiting gut microbes from the environment.

    In addition to amphipods, deep-sea fish were discovered in hadal zones half a century ago, including the deep-sea fish Pseudoliparis amblystomopsis (Andriyashev 1953), that populates the Japan Trench, and Abyssobrotula galatheae (Nielsen 1977), which was retrieved from a depth of 3100-8370 m in the Puerto Rico Trench in 1970, and holds the record for the fish found in the deepest water. Recent technological advances have generated a new wave of deep-sea exploration, resulting in the discovery of many hadal animal species, including the hadal munnopsid isopod Rectisura cf. herculean, reported from the Japan Trench (Jamieson et al. 2012), the stalked crinoids attributed to the family Hyocrinidae, reported from the hadal zones in the Southern Ocean (Roux 2015), the snailfish Pseudoliparis swirei, found below a depth of 6000 m in the Mariana Trench (Gerringer et al. 2017), the blind deep-sea mysid Amblyops magnus, from the Mariana Trench (Kou et al. 2018), the sea cucumber Benthodytes marianensis, collected from the Mariana Trench (Mu et al. 2018), and the hadal sea cucumber Paelopatides sp. from the Mariana Trench (Li et al. 2019). The gut microbiota of a hadal sea cucumber from a depth of 6140 m in the Mariana Trench was investigated and a nearly complete genome of the dominant microbe, Candidatus Spiroplasma holothuricola, was reconstructed (He et al. 2018). One striking feature of this bacterial genome is the presence of 76 clustered, regularly interspaced, short palindromic repeats that may have a protective function against invading viruses that are the main components of benthic organisms and would be very important to the host (He et al. 2018). However, apart from amphipods and sea cucumbers, little is known about the gut microbiota of other hadal animals.

Technological developments in hadal microbial studies
  • The key element in hadal zone exploration has been the development of vessels and submersible techniques (Table 1). In 1964, Alvin was built by the United States with a maximum dive depth capability of 1829 m. After continuous modification, its working depth was extended to 4500 m, which is still currently the most frequently dived depth. It retains the record for the longest stay on the seabed and is the most efficient manned submersible in the world (Kohnen 2009). In addition to vessels from the United States, the Nautile manned submersible developed by France was unveiled in 1985, with a maximum diving depth of 6000 m (Jarry 1986; Kohnen 2009). In 1987, Russia built two 6000-m-class submersibles MIR-I and MIR-II, which were the first submersibles that could cooperate with each other (Sagalevitch 1998). The Shinkai 6500 manned submersible built by Japan in 1989 dove to a depth of 6527 m. The underwater operation time was eight hours, setting a record for deep diving by manned submersibles at that time (Iwai et al. 1990; Komuku et al. 2007). In 1995, the Japanese Kaiko dove to a depth of 11, 000 m in the Challenger Deep and was the first unmanned submersible to reach the bottom of the Challenger Deep (Momma et al. 2004). In 2009, the Nereus unmanned submersible of the United States successfully reached this area after diving 10, 972 m (Bowen et al. 2009). In 2012, the Deepsea Challenger driven by James Cameron, the famous film director, became the next manned submersible after Trieste to reach the bottom of the Challenger Deep and collect samples (Hardy et al. 2013). During a second wave of deep-sea exploration, the Jiaolong manned submersible, a submersible that can take scientists to work down to 7000 m depth, was designed by China in 2012 (Cui 2013). In 2016, the Chinese 'Tan Suo Yi Hao' (Lian et al. 2020) scientific research ship successfully returned from the Mariana Trench after 'knocking on the door' of the 10, 000-m abyss. The abyss on board landers 'Tian Ya Hao' and 'Hai Jiao Hao' reached a depth of nearly 7000 m, and the self-developed 10, 000-m autonomous remote-controlled submersible 'Haidou-1' successfully dove to 10, 767 m to collect samples and data. In addition, China's newly developed manned submersible 'Fen Dou Zhe' set a national diving record of 10, 909 m in November 2020.

    Time Representative vehicle Main record
    1960 Trieste manned bathyscaphe (Italy) The first manned submersible to reach the bottom (10, 916 m) of the Challenger Deep
    1964 Alvin manned submersible (USA) It was unveiled, with a maximum dive depth of 4500 m
    1985 Nautile manned submersible (France) It was unveiled, with a maximum diving depth of 6000 m
    1987 MIR-I and MIR-II manned submersible (Russia) They were 6000-m-class submersibles that could cooperate with each other
    1989 Shinkai manned submersible (Japan) It dove to 6500 m and the underwater operation time was eight hours
    1995 Kaiko unmanned submersible (Japan) The first unmanned submersible to reach the bottom of the Challenger Deep
    2009 Nereus unmanned submersible (USA) The second unmanned submersible to reach the bottom of the Challenger Deep
    2012 Deepsea Challenger manned submersible (USA) The second manned submersible to reach the bottom of the Challenger Deep
    2012 Jiaolong manned submersible (China) Dove the maximum depth to 7062 m
    2016 Haidou-1 unmanned submersible (China) Dove to 10, 767 m to collect samples and data
    2020 Fendouzhe manned submersibl (China) Set a national diving record of 10, 909 m in November 2020

    Table 1.  Time frame of the development of the hadal exploring vessels and equipment, and main research progress

    The sampling equipment used in the early days included grabs and corers that were deployed via a wire to collect sediment samples from the seafloor. The hydro-rod corer, or the Baillie rod corer, is possibly the earliest tool used to collect sediment samples from the hadal seafloor (Wolff 1956). Yayanos (1978) and Hessler et al. (1978) reported on surveys that combined a gas-filled hydraulic accumulator, thermal insulation, and a pumping system to trap amphipods in the Marianas Trench at a depth of approximately 10, 500 m (Yayanos et al. 1979). Later, baited traps and other associated equipment attached to the landers were used to capture fish and shrimps. For example, Jamieson et al. (2009) used an imaging lander containing a video system to observe the time course of bait interception and consumption. Landers can also be equipped with sensors for conductivity, temperature, and depth. The Japan Marine Science & Technology Center (JAMSTEC) developed an 11, 000 m class free-fall mooring system to take images and sediment samples (Yoshida et al. 2009). The system consisted of a sampling launcher that contained water and sediment samplers and a pre-observation probe vehicle, which was used for preliminary surveys. The Automatic Bottom Inspector and Sampling Mobile (ABISMO) system, consisting of a ship-side system, a launcher, a vehicle, and two samplers, is a full-ocean depth remotely operated vehicle (ROV) that can collect sediment and water samples (Yoshida et al. 2009). The free-falling vehicle (FFV) was designed and constructed by National Geographic Remote Imaging and was used to collect seawater, amphipods and sediment samples at a substantial depth (Leon-Zayas et al. 2015). The core of FFV contains a camera, 3600-lm light-emitting diode arrays, and a custom embedded computer encased in a borosilicate glass sphere with a depth rating of 12, 000 m. An external pressure gauge is used to measure the final depth that the system reaches. In 2017, Wu et al. (2018) designed a gas-tight pair sampler to collect gas-tight fluid samples from the hadal zone. The sampler can be widely used on manned submersibles owing to its ability to resist ultrahigh pressure and having substantial performance of bidirectional sealing (Wu et al. 2018). With regards to maintaining the in situ pressure, Garel et al. (2019) proposed a ready-to-use pressure-holding sampler that could recover samples under in situ pressure to obtain effectively sealed and pollution-free seawater samples. In addition, to maintain the in situ status of the collected hadal microbial communities, Wang et al. (2019b) developed an in situ microbial filtration and fixation apparatus to collect hadal water. Samples obtained by this method are composed of more heterotrophic Marinimicrobia compared with those sampled by Niskin bottles (Gao et al. 2019; Wang et al. 2019b).

    After sampling, hadal microbes are typically studied using culture-independent methods. In the early twenty-first century, initial pioneering studies using 16S rRNA gene analyses, followed by metagenomics, were performed to profile the taxonomic structures of microbial communities (Kato et al. 1997; Li et al. 1999; Luo et al. 2015; Nunoura et al. 2013). These methods have expanded the understanding of hadal microbial lifestyles (Lian et al. 2020; Smedile et al. 2013; Zhang et al. 2018b, 2019b). Another challenge in the study of hadal microbiota is laboratory microbial cultivation. Most microbes known to thrive in hadal waters are facultative anaerobes that can endure high pressures (Pathom-Aree et al. 2006a; Zhao et al. 2020). Thus, hadal sample collection is often followed by the laboratory maintenance of high-pressure environments, with some also requiring an anaerobic environment. Currently, high-pressure culture devices are primarily composed of a pressurizing device, a pressure-resistant container, and a culture device (Fichtel et al. 2015). The pressurizing devices are often hydraulic pumps, and the containers are primarily made of steel to withstand the high pressures. Various types of culture devices suit different research needs. Some research utilizes airtight bags (Liu et al. 2020b; Wang et al. 2014), while others utilize sealed glass bottles to easily measure the optical density with a spectrophotometer (Scoma et al. 2019).

    When transferred to the laboratory, the culture are typically filled with nitrogen or other gasses and the analyses performed in specially constructed chambers that maintain anaerobic conditions and high pressures. However, only a few microorganisms of natural communities can be cultured. The isolated species are primarily limited to Actinobacteria [e.g., Dermacoccus abyssi (Pathom-Aree et al. 2006a), Dermacoccus barathri and Dermacoccus profundi (Pathom-Aree et al. 2006c), Williamsia marianensis (Pathom-Aree et al. 2006b), and Corynebacterium hadale (Wei et al. 2018a)], Bacteroidetes [e.g., Euzebyella marina (Liu et al. 2019a) and Winogradskyella ouciana (He et al. 2021)], Firmicutes [e.g., Thermaerobacter marianensis (Takai et al. 1999) and Bacillus piezotolerans (Yu et al. 2019a)], and Proteobacteria [e.g., Psychromonas kaikoae (Nogi et al. 2002), Colwellia piezophila (Nogi et al. 2004), Psychromonas hadalis (Nogi et al. 2007), Colwellia marinimaniae (Kusube et al. 2017), Pseudomonas abyssi (Wei et al. 2018b), Halomonas piezotolerans (Yan et al. 2020), Marinomonas piezotolerans (Yu et al. 2019b), Altererythrobacter aerophilus (Meng et al. 2019), Paraoceanicella profunda (Liu et al. 2020a), Pelagovum pacificum (Ren et al. 2020), and Marinifaba aquimaris (Sui et al. 2021)]. In addition, Liu et al. (2018) studied the diversity of cultivable bacteria in the water column at different depths of the New Britain Trench; Peoples et al. (2019) isolated a total of 50 strains, including members of Colwellia, Shewanella, Moritella, and Psychromonas, althrough the natural sediments were incubated under static, long-term, unamended high-pressure conditions. Although a variety of these isolated bacteria have been demonstrated to be piezophiles (Nogi et al. 2002, 2004), abundance estimates indicate that culturable piezophiles make up only a small fraction of hadal seawater communities (Eloe et al. 2011; Peoples et al. 2018). Therefore, from this perspective, the majority of the hadal microbial sphere remains a mystery.

Summary and future perspectives
  • We highlighted the discovery of alkanes and endogenous polysaccharide cycling as important carbon sources at the bottom of trenches. The unique structure of cell membranes, as well as the accumulation of osmolytes, facilitate microbial-cell adaptation to high hydrostatic pressures. With the development of sampling techniques and culture-independent methods for microbial study, unprecedented progress has been achieved in understanding microbial life in the hadal zone. However, several important issues remain to be resolved. For example, the role of high hydrostatic pressure in determining the vertical distribution of microbes is largely unknown, although hydrostatic pressure is hypothesized to modify bacterioplankton diversity and metabolism. The mechanisms that govern the utilization of complex carbohydrates by microbes, such as how they maintain their activity under extreme hydrostatic pressures, remain unclear. The functions that underpin the symbioses between microbes and animals in the hadal zone await in-depth and widespread investigations, which may lead to the discovery of novel lifestyles. Furthermore, an important microbial living state-biofilm formation has been widely recognized as a protective strategy against extreme conditions (Carvalho and Carla 2018; Ramírez et al. 2019). A number of unknown microbial taxa have recently been reported in marine biofilms from around the world (Zhang et al. 2019a). Future research should focus on the ecological significance of microbial biofilm formation in the hadal zone.

Acknowledgements
  • This work was supported by funding from the National Key Research & Development Program of China (Grant no. 2018YFC0310600 and 2018YFC0309904), the Fundamental Research Funds of Ocean University of China (842041010), the National Science Foundation of China (31630012, U1706207, 91851205, and 31870052), the Major Scientific and Technological Innovation Project of Shandong Province (2019JZZY010817), the Taishan Scholars Program of Shandong Province (tspd20181203), and the Fundamental Research Funds for the Central Universities (201961018).

Author Contributions
  • WZ and YZZ provided the idea of this review; SF, MW, WD and WZ drafted this manuscript; WZ, YZZ, YXL and WD revised this manuscript; WZ and SF collected and drew figures and tables. The final manuscript was approved by all of the authors.

Declarations

    Conflict of interest

  • The authors declare they have no conflict of interest. Yu-Zhong Zhang was not involved in the journal’s review of, or decisions related to this manuscript.

  • Animal and human rights statement

  • This article does not contain any studies involving human subjects or animals performed by any of the authors.

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