Impact of Sediment Plume on Benthic Microbial Community in Deep-Sea Mining

Abstract

Deep-sea polymetallic nodule provinces harbor rich benthic microbial communities that underpin biogeochemical cycles and sustain abyssal ecosystem functions. Recent studies have begun to map their abundance, diversity and community structure, emphasizing the role of environmental gradients and spatial heterogeneity. Yet the spatiotemporal dynamics and assembly mechanisms of these microbes remain largely unresolved. Mining-induced sediment plumes further complicate the picture: they modify microbial biomass, activity and composition, but the trajectories of community succession and the functional consequences of disturbance are still unclear. Thresholds used to gauge plume impacts also differ markedly among studies, hampering consistent risk assessments. In summary, a stark contrast exists between the limited in situ observational data, the widely varying impact thresholds reported across studies, and the pressing need for unified standards in environmental impact assessments for deep-sea mining. It recommends future work that integrates multi-omics, time-series in situ monitoring, cross-regional comparisons and standardized evaluation frameworks to refine microbial indicators and ecological thresholds for deep-sea mining impact assessments.

1. Introduction

With the rapid development of the global economy and the increasing depletion of terrestrial mineral resources, attention has shifted toward the vast mineral reserves hidden in the deep ocean [1,2]. Since the 1950s, numerous countries have conducted extensive exploration and discovered that the international deep-sea seabed harbors abundant solid mineral resources, including polymetallic nodules, cobalt-rich crusts, polymetallic sulfides, and rare earth elements. Polymetallic nodules, also known as ferromanganese nodules or manganese nodules, contain over 70 elements such as manganese (Mn), copper (Cu), cobalt (Co), and nickel (Ni). They are primarily found on the surface of deep-sea sediments at depths of 4000 to 6000 m [3]. Polymetallic nodules are widely distributed in the ocean basins of the Pacific and Indian Oceans, with the most well-known concentration found in the Clarion–Clipperton Zone (CCZ) of the eastern Pacific. Exploration estimates suggest that the global total polymetallic nodule resource on the ocean floor is approximately 3000 × 10⁹ t, with commercially viable reserves reaching 75 × 10⁹ t. The coverage area of polymetallic nodules on the ocean floor is approximately 54 × 10⁶ km² [4]. The elements enriched in polymetallic nodules, such as Co, Mn and Ni, are crucial components in the production of high-quality steel, advanced technology products and green energy industries. These elements are considered strategic resources. As international economic and political landscapes become increasingly complex, countries worldwide have initiated comprehensive research on the exploration and mining of deep-sea polymetallic nodules as part of their strategic resource reserves. To date, the International Seabed Authority (ISA) has signed 30 valid contracts with 20 countries for the exploration of polymetallic nodules, polymetallic sulfides, and ferromanganese crusts in the Indian Ocean, the Mid-Atlantic Ridge, and the Pacific Ocean [2].

As shown in Figure 1a, the polymetallic nodule mining system consists of a surface mining vessel, riser pipelines and a seabed mining vehicle. The mining process includes the collection of polymetallic nodules from the seafloor, vertical hydraulic transport through pipelines, mineral–water separation on the mining vessel, and transportation to land. During polymetallic nodule mining, both the collection and movement of the seabed mining vehicle disturb the seafloor sediments [5,6], causing resuspension and dispersion of the surface sediment. This process generates a sediment plume, which, driven by hydrodynamic forces, can spread over long distances before eventually settling (Figure 1b). During the generation and re-sedimentation of sediment plumes, significant changes occur at the sediment–water interface in parameters such as natural electric potential and redox potential [7,8]. In addition, the concentrations of nutrients and trace metals in bottom water are also altered [9,10]. Plume re-sedimentation can cover the surface of polymetallic nodules, thereby obstructing the carbon fixation functions of surface-associated microorganisms [11]. It may also bury benthic organisms and destroy their habitats [12]. Furthermore, as sediment plumes disperse over distances ranging from hundreds to even thousands of meters, the particle size distribution of the resuspended material may shift toward either finer or coarser fractions. This can alter the composition and grain size of seafloor sediments. Over time, large-scale deep-sea mining activities may significantly modify the sediment characteristics and geomorphology within and around the mining areas [12]. Consequently, plume re-sedimentation during polymetallic nodule mining may directly or indirectly exert negative impacts on deep-sea biodiversity and ecosystem [13,14,15,16].

Benthic microorganisms are central drivers of energy flow and biogeochemical cycling in deep-sea ecosystems. They perform essential functions such as primary production (e.g., chemoautotrophic carbon fixation by sulfur-oxidizing bacteria like Thiomicrospira and ammonia-oxidizing archaea), organic matter degradation (e.g., carbon remineralization by heterotrophic bacterial groups such as Pseudomonas and Bacteroidetes), and the cycling of key elements including nitrogen (mediated by nitrifying and denitrifying microbes) and sulfur (driven by sulfate-reducing bacteria like Desulfovibrio and sulfur-oxidizers) [17]. Their metabolic activities directly support the survival of lower trophic level organisms, such as small benthic fauna. In addition, benthic microbes play a role in the formation and maintenance of deep-sea polymetallic nodules [18]. Moreover, benthic microorganisms respond rapidly to changes in physicochemical conditions. Therefore, characterizing and monitoring benthic microbial communities before and after mining activities are essential for assessing potential environmental changes associated with polymetallic nodule mining plumes [19]. However, a major challenge remains: microbial community structure and function are shaped by a complex array of natural environmental factors—such as bottom-current velocity, topography, sediment properties, and organic matter flux—while the dispersion and sedimentation of mining-induced plumes are also modulated by these same physical and chemical conditions. Therefore, understanding the impacts of sediment plumes on benthic microbial communities, as well as the vulnerability and recovery potential of deep-sea microbial ecosystems, represents a key focus and major challenge in current research on the environmental impacts of deep-sea mining. Such knowledge is critical for predicting the extent of microbial community disturbance and the trajectory of ecosystem recovery following mining activities [9]. It also forms the foundation for developing environmentally friendly and sustainable deep-sea resource exploitation strategies, enabling a long-term balance between resource utilization and ecological conservation.

2. Distribution Characteristics of Benthic Microorganisms in Polymetallic Nodule Areas

2.1. Spatial Distribution Characteristics of Microbial Communities in Sediments of Polymetallic Nodule Areas

Polymetallic nodules are primarily distributed in regions such as the CCZ and the Peru Basin in the eastern Pacific, seamounts in parts of the western Pacific, the Central Indian Ocean Basin and the Mid-Atlantic Ridge. In recent years, researchers have gradually begun to investigate the microbial communities in sediments from polymetallic nodule areas across these different regions. The results of these studies are summarized in Table 1. Molari et al. [20] found that the dominant microbial taxa in sediments from the polymetallic nodule region of the Peru Basin primarily belong to the classes γ-Pseudomonadota, α-Pseudomonadota, δ-Pseudomonadota, and Acidimicrobiia. Similarly, Jing et al. [21] identified γ-Pseudomonadota and Bacillota as the dominant groups in sediments from the polymetallic nodule region of the eastern Pacific. Shah et al. [22] reported that in the Central Indian Ocean Basin, the predominant phyla in nodule-bearing sediments include Bacillota, Actinobacteria and Bacteroidetes. Zeng [23] reported that surface sediments in the polymetallic nodule region of the western Pacific are dominated by microorganisms belonging to the phyla γ-Pseudomonadota, α-Pseudomonadota, Nitrososphaerota, Chloroflexota, Actinobacteria, Bacteroidetes, Bacillota and Acidobacteriota. Similarly, Sun et al. [24] found that the dominant phyla in sediments from the same region include Pseudomonadota (32–82%), Thermoproteota (4–37%), Bacillota (2–18%) and Mortierellomycota (1–6%). Zhang [25] found that bacteria cultivable under laboratory conditions from sediments in the polymetallic nodule region of the western Pacific primarily belong to the classes α-Pseudomonadota and γ-Pseudomonadota. Chen et al. [26] reported the presence of bacterial groups with potential humic substance transformation capabilities in the same region, including members of the classes Actinobacteria, Fibrobacteria, Flavobacteria, α-Pseudomonadota, and γ-Pseudomonadota. Wang et al. [27] identified Pseudomonadota as the dominant microbial group in sediments from the Marcus-Wake seamount polymetallic nodule area in the western Pacific. Based on previous studies of sediment microbial communities across different polymetallic nodule regions, some researchers have further investigated the spatial distribution of microbes in sediments from varying seafloor geomorphologies within the same nodule field, as well as their vertical distribution along sediment depth profiles. Lejzerowicz et al. [28] found that in the CCZ, benthic eukaryotes exhibited higher abundance and spatial heterogeneity in depressions compared to slope areas. Peng et al. [29] reported that surface sediments (0–1 cm) had significantly higher species richness, diversity, and evenness than deeper layers (35–36 cm), highlighting the pronounced spatial heterogeneity of microbial communities in polymetallic nodule-bearing sediments. Similarly, Sun et al. [24] found that prokaryotic diversity in surface sediments (0–8 cm) was more than four times higher than that in deeper layers (8–26 cm). They also observed that deterministic processes primarily shaped the structure of surface prokaryotic communities, whereas stochastic processes played a greater role at depth. The co-occurrence networks of surface prokaryotes were more complex, and sediment depth emerged as a key factor governing microbial distribution. In addition, heavy metals such as iron, copper, nickel, cobalt and zinc were found to significantly influence the vertical distribution of prokaryotic communities. In addition, researchers have observed that the composition of microbial communities in sediments varies significantly with depth, gradually reaching a stable state below 10 cm [30].

Numerous studies have revealed significant spatial heterogeneity in the distribution of archaea within sediments and polymetallic nodules from deep-sea environments. Shulse et al. [31] found that archaea accounted for 24% of the total prokaryotic community, with Thaumarchaeota being the dominant phylum. In the South Pacific Gyre, Tully et al. [32] reported even higher archaeal abundances in polymetallic nodules, with relative abundances exceeding 50% in some cases. However, such high archaeal abundance is not globally consistent. For example, Molari et al. [20] reported a maximum archaeal abundance of only 7% in nodules from the Peru Basin, attributing the lower abundance to higher particle fluxes and ammonium availability in that region. Similarly, Zhang et al. [33] observed an extremely low relative abundance (0.01%) of Nitrosopumilus in nodules from seamounts. Furthermore, a comparative study by Bergo et al. [34] found that both the diversity and abundance of archaea in ferromanganese crusts and nodules from the Atlantic Ocean were significantly lower than those in the Pacific.

Overall, previous studies have shown that microbial biomass and spatial heterogeneity are generally higher in depressions compared to slope regions. Vertically, microbial diversity and the complexity of interspecies interactions both decrease with increasing sediment depth. The mechanisms shaping microbial community assembly also shift with depth: surface communities are primarily driven by deterministic processes, such as environmental selection, while deeper communities are more influenced by stochastic processes. Sediment depth and its associated heavy metal content are key environmental factors underlying this vertical stratification. Despite significant spatial heterogeneity in benthic microbial communities within polymetallic nodule fields, several dominant taxa are consistently observed across different ocean regions. These include members of the Pseudomonadota, Bacillota, Actinobacteria, Bacteroidetes, Chloroflexota and Planctomycetota. These microbes play essential roles in the oligotrophic, metal-rich deep-sea environment, contributing to functions such as metal redox cycling, organic matter degradation, and stress-resistance metabolism. For instance, chemolithoautotrophic and methylotrophic groups within γ-Pseudomonadota and α-Pseudomonadota are involved in carbon and nitrogen transformations, while members of Chloroflexota participate in nitrogen cycling.

Table 1. Dominant microbial taxa in sediments from different polymetallic nodule areas.

Area		Dominant Taxa	References
Location	Longitude and Latitude
Eastern Pacific Ocean		γ-Pseudomonadota, α-Pseudomonadota, δ-Pseudomonadota and Acidimicrobiia	[20]
		Burkholderiales, Pseudomonadales, Nitrosopumilales	[30]
		Pseudomonadota and Bacillota	[21]
Western Pacific Ocean		Nitrosopumilus, Sphingomonas, Woeseia and Ralstonia	[35]
		γ-Pseudomonadota (49.8%), α-Pseudomonadota (4.9%), Actinobacteriota (15.5%), Bacteroidota (11.9%), Bacillota (4.2%), Chloroflexota (3.6%), Thermoproteota (3.0%) and Acidobacteriota (2.0%)	[23]
		Pseudomonadota (32–82%), Archaea (4–37%), Bacillota (2–18%) and Water mold (1–6%)	[24]
		α-Pseudomonadota (35.8%), γ-Pseudomonadota (35.3%), Bacillota (14.7%), Actinomycetes (14.32%)	[25]
	157.03°–161.09° E, 20.02°–23.18° N	Actinobacteria, Bacillota, Flavobacterium, α-Pseudomonadota and γ-Pseudomonadota	[26]
	155°–160° E, 19°–21° N	α-Pseudomonadota (24.76%), γ-Pseudomonadota (20.21%), δ-Pseudomonadota (6.48%), Chloroflexota, Acidobacteriota, Gemmatimonas, Planctomycetota, Actinobacteria, Bacteroidetes and Nitrospirae	[27]
Indian Ocean	(12.4° S, 75.33° E), (12.56° S, 74.41° E) (13.4° S, 75.33° E)	Bacillota, Actinobacteria and Bacteroidota. Sediments below 10 cm are dominated by Bacillota.	[22]

Table 1. Dominant microbial taxa in sediments from different polymetallic nodule areas.

Area		Dominant Taxa	References
Location	Longitude and Latitude
Eastern Pacific Ocean		γ-Pseudomonadota, α-Pseudomonadota, δ-Pseudomonadota and Acidimicrobiia	[20]
		Burkholderiales, Pseudomonadales, Nitrosopumilales	[30]
		Pseudomonadota and Bacillota	[21]
Western Pacific Ocean		Nitrosopumilus, Sphingomonas, Woeseia and Ralstonia	[35]
		γ-Pseudomonadota (49.8%), α-Pseudomonadota (4.9%), Actinobacteriota (15.5%), Bacteroidota (11.9%), Bacillota (4.2%), Chloroflexota (3.6%), Thermoproteota (3.0%) and Acidobacteriota (2.0%)	[23]
		Pseudomonadota (32–82%), Archaea (4–37%), Bacillota (2–18%) and Water mold (1–6%)	[24]
		α-Pseudomonadota (35.8%), γ-Pseudomonadota (35.3%), Bacillota (14.7%), Actinomycetes (14.32%)	[25]
	157.03°–161.09° E, 20.02°–23.18° N	Actinobacteria, Bacillota, Flavobacterium, α-Pseudomonadota and γ-Pseudomonadota	[26]
	155°–160° E, 19°–21° N	α-Pseudomonadota (24.76%), γ-Pseudomonadota (20.21%), δ-Pseudomonadota (6.48%), Chloroflexota, Acidobacteriota, Gemmatimonas, Planctomycetota, Actinobacteria, Bacteroidetes and Nitrospirae	[27]
Indian Ocean	(12.4° S, 75.33° E), (12.56° S, 74.41° E) (13.4° S, 75.33° E)	Bacillota, Actinobacteria and Bacteroidota. Sediments below 10 cm are dominated by Bacillota.	[22]

2.2. Comparison of Microbial Communities in the Water Column, Polymetallic Nodules and Sediments of Polymetallic Nodule Areas

In addition, some researchers have conducted comparative studies on microbial distributions in non-nodule sediments, nodule-bearing sediments, the water column, and both the interior and exterior of polymetallic nodules within the same marine region. Li et al. [36] reported that bacterial community structures in sediment samples containing nodules differed significantly from those in sediments lacking nodules. Lindh et al. [37] investigated the distribution of microorganisms in the water column, sediments and nodules in the CCZ and found that γ-Pseudomonadota and α-Pseudomonadota were more abundant in both sediments and nodules compared to the overlying water column. Furthermore, the relative abundances of OTUs belonging to the Rhodobacteraceae family and Vibrio genus were higher in nodules than in sediments and the water column. Comparative studies on microbial communities within polymetallic nodules and in surrounding sediments have revealed distinct patterns. Shiraishi et al. [38] found that microbial abundance inside polymetallic nodules was up to three orders of magnitude higher than in adjacent sediments. However, Shulse et al. [31] and Tully et al. [32] reported that microbial diversity in sediments was significantly higher than within the nodules. Similarly, Wu et al. [39] observed that bacterial diversity in sediments exceeded that of nodule interiors, while archaeal diversity was lower in sediments compared to nodules. Furthermore, Jiang et al. [40] found that surface sediments exhibited greater bacterial diversity and more active biogeochemical processes than the interiors of polymetallic nodules.

Archaeal community structures vary significantly across different habitats. Molari et al. [20] clearly demonstrated habitat specificity, reporting that archaeal abundance in sediments from the Peru Basin reached up to 45%, while it remained much lower in nodules (<1–7%). Tully et al. [32] further highlighted microhabitat-level variation, showing that even within polymetallic nodules, the Thaumarchaeota MG-1 group exhibited high OTU-level microdiversity, with community composition differing between the inner and outer nodule layers. In the water column, Shah et al. [22] found a distinct archaeal community composition compared to sediments. Specifically, Thermoplasmata dominated the water column, while Nitrososphaeria prevailed in the sediments.

In summary, these comparative studies consistently indicate that polymetallic nodules are not isolated microbial habitats, but rather part of a complex ecosystem that includes surrounding sediments and overlying water, characterized by pronounced habitat heterogeneity. While nodules may support high-density growth of specific microbial taxa, their overall microbial diversity is typically lower than that of surrounding sediments. This may be attributed to the nodules’ limited resource availability and physically complex structure. Such differences suggest that nodules and sediments may play complementary, rather than redundant, ecological roles in microbial functioning and biogeochemical cycling.

2.3. Metabolic and Ecological Functions of Benthic Microorganisms in Polymetallic Nodule Areas

Furthermore, researchers have investigated the functional characteristics of microbial communities in sediments from polymetallic nodule regions. Numerous studies have shown that these microorganisms not only participate in fundamental metabolic processes but also play critical roles in the cycling of key elements unique to the deep-sea environment. Wang et al. [27] reported that microbial communities in sediments from the Marcus-Wake seamount polymetallic nodule area in the western Pacific were primarily involved in signal transduction, protein transport, prokaryotic carbon fixation, quorum sensing, energy conversion, as well as amino acid and pyrimidine metabolism. Cecchetto et al. [41] found that bacteria in nodule-bearing sediments played a dominant role in the short-term (approximately 1.5 days) uptake of organic carbon on the seafloor. Concerning resistance mechanisms against heavy metal toxicity, Zhang et al. [33] found that within these metal-rich sediment environments, heterotrophic and chemolithoautotrophic microorganisms had developed mechanisms of resistance to heavy metals including metal efflux (Mn, Cu, As, and Pb), adsorption uptake (Fe, Cu, Zn, Pb, and Hg) and metal biotransformation by enzymatic redox (Mn, Fe, Cu, As, Cr, and Hg). They speculate that inorganic nutrients oxidation may constitute a very important way for many of these microorganisms to obtain energy. These mechanisms not only ensure microbial survival under metal-induced stress but also suggest that energy acquisition may be coupled with metal redox processes. In such environments, the oxidation of inorganic substrates could serve as a significant energy source. Moreover, certain microbial groups may play potential roles in the formation of polymetallic nodules. Cho et al. [19] has found that Hyphomiocrobium and Aurantimonas in α-Pseudomonadota, as well as Marinobacteria in γ-Pseudomonadota, play important roles in the formation of nodules and manganese nodules in the Korea Deep Ocean Study region are mainly formed by oxidative diagenesis processes.

Both Molari et al. [20] reported that archaeal communities were almost exclusively dominated by the order Nitrosopumilales. These ammonia-oxidizing archaea are key initiators of deep-sea nitrification, capable of oxidizing ammonia to nitrite. Tully et al. [32] further hypothesized that these archaea act as chemolithoautotrophic primary producers in the oligotrophic deep-sea environment, supplying energy and carbon to the local food web through ammonia oxidation and carbon fixation. Beyond their core role in nitrogen cycling, Shiraishi et al. [38] suggested that members of the phylum Thaumarchaeota may participate in manganese oxidation via multicopper oxidases. Additionally, Xu et al. [42] proposed that archaea might also be involved in sulfur disproportionation, highlighting their potential roles in both metal and sulfur cycling.

Overall, benthic microorganisms in polymetallic nodule areas exhibit functional adaptations to the deep sea’s oligotrophic and metal-rich environment. On one hand, they sustain the community’s energy foundation through efficient carbon fixation and organic matter metabolism. On the other, they have evolved diverse mechanisms for heavy metal resistance and transformation. Certain taxa may also directly contribute to mineral formation. Together, these functional traits shape the unique ecological niches of microorganisms in such habitats and underscore their significant, and often underappreciated, role in driving global deep-sea biogeochemical cycles.

3. Impacts of Sediment Plumes on Benthic Microbial Community During Polymetallic Nodule Mining

3.1. In Situ Deep-Sea Experiments on the Effects of Sediment Plumes on Benthic Microbial Community

Sediment plumes have significant impacts on deep-sea ecosystems. Some researchers have conducted studies on the effects of plumes on small benthic organisms. Mevenkamp et al. [43] found that when the thickness of the fragmented nodule particle layer reached 2 cm, significant changes occurred within 11 days in the vertical distribution of small benthic fauna and the proportion of nematode feeding types in the sediment. Some researchers have also explored the impacts of sediment plumes on benthic microbial communities. Based on a deep-sea mining in situ disturbance experiment conducted by Germany in 1989 in the Peru Basin of the South Pacific. Vonnahme et al. [44] studied benthic microbes in the region. Their findings showed that microbial biomass decreased by 50% five weeks after the disturbance, by less than 30% after 26 years, and that microbial activity had declined fourfold after 50 years. Based on results from deep-sea mining in situ disturbance experiments and studies on the impacts of plumes from other seafloor activities, Vonnahme et al. [44] estimated that microbially mediated biogeochemical functions may take more than 50 years to return to pre-disturbance levels following polymetallic nodule mining. In contrast, Haffert et al. [8] estimated, using typical deep-sea microbial biomass turnover rates and conservative bacterial doubling times, that microbial abundance could recover within 2 to 10 years after mining. De Jonge et al. [45] found that, 26 years after a small-scale sediment disturbance, the total carbon flux within the impacted area remained 16% lower compared to a reference site. Notably, carbon cycling within the microbial loop was reduced by 35%. While faunal respiration had recovered—and in some cases exceeded—baseline levels, recovery varied significantly across different taxonomic groups. The authors further recommend that, in addition to faunal monitoring, indicators such as sediment integrity and prokaryotic production should be included as complementary metrics for assessing the ecological status of abyssal ecosystems. A follow-up investigation conducted in 2023 revisited the in situ deep-sea mining disturbance experiment initiated by Germany in 1989 in the Peru Basin of the South Pacific [46]. The study revealed that, even after 44 years, visible physical disturbance marks remain, with little evidence of natural physical recovery. Notably, mobile fauna were still present in the most heavily disturbed areas, and the densities of macrofauna associated with sediments or nodules, as well as microbial biomass, were comparable between disturbed and undisturbed zones. Furthermore, the findings indicate that some sessile megafauna have begun early-stage recolonization after four decades. Although sediment plumes generated by the mining vehicle are no longer visually apparent, light reflectance measurements still detect infilling of sediments between nodules. Interestingly, the disturbed areas exhibited higher megafaunal densities than adjacent undisturbed regions. The study concludes that visible physical impacts from deep-sea mining activities are likely to persist for several decades. This contrasts with the long-term functional impairments reported by Vonnahme et al. [44] and De Jonge et al. [45], who found a 16% reduction in total carbon flux and a 35% decline in microbial activity 26 years after disturbance. These noticeable differences could stem from several factors: Disturbance scale and intensity: The Ocean Minerals Company (OMCO) experiment was a single, small-scale event, while the Disturbance and Recolonization Experiment (DISCOL) involved repeated disturbances across a larger area. Recovery assessment metrics: Jones et al. [46] focused on density and biomass, whereas Vonnahme et al. [44] and De Jonge et al. [45] emphasized biogeochemical functions, which may be more sensitive to ongoing changes in sediment structure and organic matter availability. Environmental heterogeneity: Unlike the nutrient-rich Peru Basin, the nutrient-poor CCZ may exhibit different recovery dynamics, which can influence nutrient cycling and community reassembly.

Current research on the impacts of sediment plumes on benthic microorganisms remains limited. Some researchers have indirectly investigated these effects by studying the influence of plumes generated by submarine landslides, hydrothermal vents, and riverine discharges on benthic microbial communities. Wang et al. [27] found that plume rsedimentation resulting from submarine landslides led to a decline in benthic bacterial community diversity and significant changes in functional groups. In a study on the dynamic effects of hydrothermal plumes, Xie et al. [47] reported that the particle deposition zone beneath the plume contained a higher abundance of Campylobacteria compared to the neutrally buoyant plume zone above. Moreover, when hydrothermal activity intensified, the relative abundance of Campylobacteria increased significantly, while that of α-Pseudomonadota decreased. Fernandes et al. [48] investigating the impact of sediment plumes released by a dam collapse on nearby marine microbial communities, found that dominant microbial taxa from the original dam area were also detected in the affected marine zones. Furthermore, the closer a site was to the dam, the higher the abundance of these dominant taxa. Using analogies from events such as submarine landslides, hydrothermal vent activity, or riverine discharges to infer the impacts of deep-sea mining plumes on benthic microbial communities has clear limitations. The core issue lies in the fundamental differences between stressors: deep-sea mining plumes represent a unique form of disturbance, characterized by physical smothering combined with specific geochemical inputs (e.g., freshly released metal particles). These plumes can act persistently, on large spatial and temporal scales, within the otherwise stable and oligotrophic deep-sea environment. In contrast, the commonly cited analogues are typically short-term, pulse-like disturbances, often accompanied by nutrient enrichment, chemical toxicity, or salinity fluctuations-each driven by different dominant factors. As a result, conclusions drawn from such analogies may severely underestimate the sensitivity of abyssal microbial communities to long-term burial and subtle geochemical perturbations. They also fail to capture the potential impacts of large-scale mining on regional community connectivity and recovery potential. While analogical studies have highlighted that sediment disturbance can significantly alter microbial communities, the specific consequences of deep-sea mining require independent assessment. These should be based on targeted experimental simulations and systematic long-term monitoring under the unique conditions of mining-impacted environments.

3.2. Shallow-Water Experimental Study on the Effects of Plumes on Benthic Microbial Community

Gillard et al. [49], through laboratory experiments, investigated the effects of sediment plumes on benthic microorganisms and found that the metal tolerance concentrations of Rhodococcus erythropolis, Loktanella cinnabarina, and Dietzia maris were 228.9, 57.2, and 14.3 mM, respectively. They further suggested that these three strains could serve as potential indicator microorganisms for metal release or plume generation during mining activities. Grient and Drazen [50] reviewed the responses of animals in various shallow-water habitats (marine, estuarine, and freshwater) to increased concentrations of suspended sediments. Based on the similarities in sensitivity to relative suspended sediment concentrations, the study estimated deep-sea sensitivity thresholds for acute exposure to elevated sediment levels in the absence of empirical data. Although existing studies indicate that ecological sensitivity based on relative sediment concentrations shows high consistency across different aquatic habitats—including marine, estuarine, and freshwater systems—providing a basis for extrapolating shallow-water data to the deep sea, significant limitations and uncertainties remain with this approach. The main limitation is that shallow-water simulations cannot replicate the extreme conditions of the deep sea, such as high pressure, low temperature, and extremely low suspended sediment concentrations. The uncertainty arises because species used in shallow-water experiments do not represent the highly specialized deep-sea communities, which are energy-limited, metabolically slow, and potentially more sensitive to sediment disturbance. Additionally, these studies do not account for the chronic exposure and combined effects of multiple pollutants unique to deep-sea mining. Therefore, predictions based on shallow-water data should be considered preliminary and require validation and refinement using deep-sea-specific data.

3.3. Sediment Plume Threshold

Sediment plumes pose a significant potential threat to the biodiversity and ecosystem functions of deep-sea environments. Defining threshold values for plume impacts is therefore critical for accurately assessing the environmental consequences of deep-sea mining. To date, several researchers have investigated plume impact thresholds through laboratory simulation experiments and numerical modeling. Stenvers et al. [51] investigated the effects of sediment plumes on jellyfish and found that when plume concentrations reached ≥17 mg/L, jellyfish responded defensively by secreting large amounts of mucus. At concentrations ≥167 mg/L, gene expression related to aerobic respiration and wound healing was triggered, indicating that the plume had caused physical damage or tissue stress. Ma et al. [52], using numerical modeling, analyzed plume deposition thickness and classified it into three levels: 0–1 mm, 1–5 mm, and 5–10 mm, with increasing levels of impact on benthic organisms. Based on existing data on the effects of sediment plumes on benthic fauna, Kaikkonen et al. [53] employed a causal and probabilistic network approach to estimate a critical deposition thickness of 2 cm—beyond which species disturbance exceeds environmentally acceptable thresholds. Grient and Drazen [50] suggest that, therefore, it is recommended to follow the precautionary principle and set the threshold for acute plume impacts very close to the natural background relative concentration of suspended solids. Current threshold studies primarily focus on model organisms (e.g., jellyfish) [51] or the overall community response [9,10]. However, it is still unclear which deep-sea taxa are most sensitive to suspended sediment concentrations. As such, a community-level estimate may serve as a reasonable starting point for setting thresholds in these ecosystems, until more specific deep-sea data becomes available.

4. Conclusions and Prospects

4.1. Conclusions

This review systematically summarizes current research on benthic microorganisms in polymetallic nodule areas and the impacts of deep-sea mining plumes on benthic microbial communities. The main conclusions are as follows:

(1)

The common microbial taxa in sediments from various polymetallic nodule regions worldwide are Pseudomonadota and Bacillota. And the benthic microbial communities exhibit strong spatial heterogeneity influenced by seafloor topography and sediment depth. However, the lack of time-series data obscures community dynamics and succession patterns. Moreover, the heavy reliance on DNA-based taxonomic profiles limits the understanding of microbes’ in situ metabolic activities and the underlying mechanisms of community assembly.

(2)

A thin sediment layer as shallow as 2 cm can rapidly alter benthic microbial community structure and suppress biogeochemical functions such as carbon cycling. Recovery of these ecological functions may take decades. Additionally, a synergistic effect between physical burial and chemical stress caused by metal leaching, which is a key factor driving the significant long-term risks of mining activities to the seafloor ecosystem. Compared to taxonomic abundance alone, microbial functional indicators provide a more sensitive measure of disturbance caused by deep-sea mining.

4.2. Prospects

(1)

Fundamental ecological research on benthic microbial communities in polymetallic nodule areas: It is recommended to systematically investigate the dynamic patterns of benthic microbial communities in polymetallic nodule regions under the influences of seasonal changes, geological evolution, and ecological succession. By integrating multi-omics approaches—including metagenomics, metatranscriptomics, and metabolomics—the project will quantify the relative contributions of environmental selection, biotic interactions, and stochastic processes in shaping community assembly. An environment–gene–ecological process coupling model will be established to reveal underlying mechanisms. Additionally, cross-regional comparative studies between the CCZ, the Indian Ocean, and other representative regions will be conducted to elucidate how geological structures, ocean current patterns, and mineral compositions influence microbial biogeographic distribution.

(2)

Ecological effects of microbial communities under sediment plume: It is proposed to conduct hierarchical investigations into the impacts of sediment plumes. First, it is recommended to establish a time-series in situ observation system using sediment traps and deep-sea landers to collect continuous samples under varying levels of disturbance. Combined with metagenomic sequencing and isotope tracing techniques, this approach aims to reveal the dynamic succession of microbial communities from initial response to post-disturbance stabilization. Second, by integrating metatranscriptomics and metabolomics, a three-dimensional analytical framework—linking species composition, functional genes, and metabolic pathways—will be developed to uncover the mechanisms by which key ecological functions such as carbon, nitrogen, and sulfur cycling are restructured under plume influence. To dissect community assembly processes, null model analysis combined with network topology metrics will be used to quantify the relative contributions of deterministic versus stochastic processes, with particular attention to niche differentiation driven by the resettlement of iron and manganese oxides. In parallel, controlled microcosm experiments are recommended. These will manipulate variables such as sediment coverage thickness, particle size, and redox gradients to explore the coupled effects of physical burial and chemical stress. Finally, a multi-parameter coupled model should be constructed to integrate plume dispersion dynamics, sediment geochemistry, and microbial response thresholds. This model will provide a theoretical foundation for developing a microbial indicator–based ecological risk assessment framework tailored to deep-sea mining impacts.

(3)

Standardization of thresholds for sediment plume: It is recommended to establish a standardized threshold framework for sediment plumes, grounded in benthic microbial ecological responses. First, a standardized indicator system should be established by coupling biogeochemical parameters—such as microbial abundance, community structure shifts, and key enzyme activities—with physical sedimentation metrics. This approach aims to overcome the limitations of current one-dimensional threshold assessments. Second, multi-scale experimental validation is essential. Laboratory simulations should be calibrated using in situ deep-sea observation data, and a three-dimensional dynamic plume model incorporating microbial physiological stress responses should be developed to address the hydrodynamic discrepancies between shallow-water simulations and actual deep-sea environments. It is also recommended to establish long-term ecological monitoring stations. These should be integrated with controlled mining trials to track changes in microbial functional gene expression and biogeochemical fluxes. From the perspective of ecosystem service functions, this will enable the construction of dose–response relationships between disturbance intensity and ecological thresholds. Finally, international collaboration should be strengthened. Comparative studies across polymetallic nodule provinces are needed to formulate tiered threshold standards—such as reversible disturbance thresholds and irreversible damage thresholds. These will provide a scientifically grounded and operationally feasible basis for environmental risk management in deep-sea mining.