International audience | Microbes are phylogenetically (Archaea, Bacteria, Eukarya, and viruses) and functionally diverse. They colonize highly varied environments and rapidly respond to and evolve as a response to local and global environmental changes, including those induced by pollutants resulting from human activities. This review exemplifies the Microbial Ecology EC2CO consortium’s efforts to explore the biology, ecology, diversity, and roles of microbes in aquatic and continental ecosystems.

Understanding the underlying mechanisms of community assembly is a major challenge in microbial ecology, particularly in communities composed of diverse organisms with different ecological characteristics. However, very little is known about the effects of marine compartments in shaping marine planktonic communities; primarily, how they are related to organism types and environmental variables. In this study, we used multiple statistical methods to explore the mechanisms driving phytoplankton and zooplankton metacommunity dynamics at the regional scale in the Bohai Sea, China. Clear geographic patterns were observed in both phytoplankton and zooplankton communities. Zooplankton showed a stronger distance-decay of similarity than phytoplankton, which had greater community differences between locations with further distances. Our analyses indicated that the zooplankton communities were primarily governed by species sorting versus dispersal limitation than the phytoplankton communities. Furthermore, we detected that zooplankton exhibited wider habitat niche breadths and dispersal abilities than phytoplankton. Our findings also showed that environmental pollution affected high trophic organisms via food webs; the presence of heavy metals in the Bohai Sea altered the abundance of some phytoplankton, and thus modified the zooplankton that feed on them.

Bacteria and archaea (prokaryotes) are vital components for maintaining healthy function of groundwater ecosystems. The prokaryotic community composition and associated putative functional processes were examined in a shallow sandy aquifer in a wet-dry tropical environment. The aquifer had a contaminated gradient of saline mine-water, which primarily consisted of elevated magnesium (Mg²⁺) and sulfate (SO₄²⁻), although other major ions and trace metals were also present. Groundwaters were sampled from piezometers, approximately 2 m in depth, located in the creek channel upstream and downstream of the mine-water influence. Sampling occurred during the dry-season when only subsurface water flow was present. Next generation sequencing was used to analyse the prokaryote assemblages using 16S rDNA and metabolic functions were predicted with FAPROTAX. Significant changes in community composition and functional processes were observed with exposure to mine-waters. Communities in the exposed sites had significantly lower relative abundance of methanotrophs such as Methylococcaceae and methanogens (Methanobacteriaceae), but higher abundance in Nitrososphaeraceae, associated with nitrification, indicating potentially important changes in the biogeochemistry of the exposed sites. The changes were most strongly correlated with concentrations of SO₄²⁻, Mg²⁺ and Na⁺. This knowledge allows an assessment of the risk of mine-water contamination to groundwater ecosystem function and aids mine-water management.

Plastisphere, an ecosystem of microbes thriving on floating plastic debris, has been extensively studied in marine waters since 2013. Currently, very little is known about the freshwater plastisphere. This review seeks to provide a broad insight into the freshwater science of plastisphere in the light of marine plastisphere, including research gaps, suggestions, and rising concerns, which would be of interest to the public, policymakers, and stakeholders. Given that freshwaters are endangered ecosystems, it is imperative to understand the role and impact of plastisphere on freshwaters. Plastic debris, especially microplastics (size <5 mm) in freshwater ecosystems, provide a stable, persistent, and buoyant substrate for microbes. Although current evidence suggests that freshwater environmental conditions and microplastics' physical and chemical properties significantly influence microbial colonisation, its role and integration in the aquatic ecosystems are unknown. Considering that the plastisphere biodiversity is unique, we seek to establish why and how many species co-exist in the plastisphere. Evaluating such fundamental questions should advance our basic understanding of the resilience of plastisphere to the changing environment. Plastisphere microbes, including the pathogenic bacteria, were found in both systems demonstrating their ability to survive on the plastic fragments from one ecosystem to another. A significant concern regarding plastisphere is the potential freshwater dispersal of anthropogenic pollutants and invasive or pathogenic species. Notably, microplastics aggregates may serve as a food source for grazers, which opens the question of the extent to which it can impact freshwater food webs. To gain a thorough understanding of the interplay between microplastics and the biogeochemical cycle, further insight into plastisphere microbes’ functional role is needed. This would shed light on the unconsidered freshwater elemental cycling pathways. Given the complexity and universal nature of the plastisphere, strong interdisciplinary global research initiatives or networks are required to address the emerging concerns of plastisphere in freshwaters.

Human activities introduce significant contamination into aquatic systems that impact biodiversity and ecosystem function. Many contaminants accumulate, and remediation options are now required worldwide. One method for bioremediation involves the application of macrofauna to stimulate microbial ecosystem processes including contaminant removal. However, if we are to confidently apply such a technique, we need clarity on the effect of bioturbators on different contaminants and how these vary under different environmental scenarios. Here we used a systematic review and meta-analysis to analyse current knowledge on the activities of bioturbating macrofauna in contaminated sediments and quantify how bioturbation-bioremediation changes depend on the taxonomic group, the aquatic ecosystem and important environmental variables. Three common contaminant classes were reviewed and analysed: metals, nutrients (i.e. ammonia and phosphorous) and polycyclic aromatic hydrocarbons (PAH). In addition, meta-regressions were calculated to estimate the effect of environmental and experimental design variables on effect sizes. Meta-analytic results revealed that deeper burrowing and more active sediment surface animals (e.g. polychaetes) increased metal release from sediments, nutrients and oxygen uptake by microbial fractions in comparison to bioturbators that inhabit shallower depths in sediments. In addition, there was a different effect of bioturbators on response variables in different aquatic systems. Finally, bioturbator effects on nutrient and metal release appeared modulated by context-specific variables such as temperature, pH, sediment grain size, animal density and experimental duration. Our findings highlight critical knowledge gaps such as field applications, less studied macrobenthic fauna and the incorporation of molecular approaches. Our results provide the first quantitative synthesis of the effects of bioturbators on contaminant fate and the variables that need to be considered for the optimization of this method as a viable approach for sediment remediation and contaminant management in aquatic systems.

Plastic pollution has now been found within multiple ecosystems across the globe. Characterisation of microbial assemblages associated with marine plastic, or the so-called ‘plastisphere’, has focused predominantly on plastic in the epipelagic zone. Whether this community includes taxa that are consistently enriched on plastic compared to surrounding non plastic surfaces is unresolved, as are the ecological implications. The deep sea is likely a final sink for most of the plastic entering the ocean, yet there is limited information on microbial colonisation of plastic at depth. The aim of this study was to investigate deep-sea microbial communities associated with polystyrene (PS) and polyurethane (PU) with Bath stone used as a control. The substrates (n = 15) were deployed in the Rockall Trough (Atlantic), and recovered 420 days later from a depth of 1796 m. To characterise the bacterial communities, 16S rRNA genes were sequenced using the Illumina MiSeq platform. A dominant core microbiome (taxa shared across all substrates) comprised 8% of total ASVs (amplicon sequence variant) and accounted for 92% of the total community reads. This suggests that many commonly reported members of the plastisphere are simply opportunistic which freely colonise any hard surface. Transiently associated species consisted of approximately 7% of the total community. Thirty genera were enriched on plastic (P < 0.05), representing 1% of the total community. The discovery of novel deep-sea enriched taxa included Aurantivirga, Algivirga, IheB3-7, Spirosoma, HTCC5015, Ekhidna and Calorithrix on PS and Candidatus Obscuribacter, Haloferula, Marine Methylotrophic Group 3, Aliivibrio, Tibeticola and Dethiosulfatarculus on PU. This small fraction of the microbiome include taxa with unique metabolic abilities and show how bacterial communities can be shaped by plastic pollution at depth. This study outlines a novel approach in categorising the plastisphere to elucidate the ecological implications of enriched taxa that show an affinity for colonising plastic.

Tetrabromobisphenol A (TBBPA) is the most used flame retardant worldwide and has become a threat to aquatic ecosystems. Previous research into the degradation of this micropollutant in anaerobic bioreactors has suggested several identities of putative TBBPA degraders. However, the organisms actively degrading TBBPA under in situ conditions have so far not been identified. Protein-stable isotope probing (protein-SIP) has become a cutting-edge technique in microbial ecology for enabling the link between identity and function under in situ conditions. Therefore, it was hypothesized that combining protein-based stable isotope probing with metagenomics could be used to identify and provide genomic insight into the TBBPA-degrading organisms. The identified ¹³C-labelled peptides were found to belong to organisms affiliated to Phytobacter, Clostridium, Sporolactobacillus, and Klebsilla genera. The functional classification of identified labelled peptides revealed that TBBPA is not only transformed by cometabolic reactions, but also assimilated into the biomass. By application of the proteogenomics with labelled micropollutants (protein-SIP) and metagenome-assembled genomes, it was possible to extend the current perspective of the diversity of TBBPA degraders in wastewater and predict putative TBBPA degradation pathways. The study provides a link to the active TBBPA degraders and which organisms to favor for optimized biodegradation.

Antibiotic resistance genes (ARGs) and virulence factors (VFs) are critical threats to human health. Their abundance in aquatic ecosystems is maintained and enhanced via selection driven by environmental xenobiotics. However, their activity and expression in these environments under xenobiotic stress remains unknown. Here ARG and VF expression profiles were examined in aquatic microcosms under ciprofloxacin, glyphosate and sertraline hydrochloride treatment. Ciprofloxacin increased total expression of ARGs, particularly multidrug resistance genes. Total expression of ARGs and VFs decreased significantly under glyphosate and sertraline treatments. However, in opportunistic human pathogens, these agents increased expression of both ARGs and VFs. Xenobiotic pollutants, such as the compounds we tested here, have the potential to disrupt microbial ecology, promote resistance, and increase risk to human health. This study systematically evaluated the effects of environmental xenobiotics on transcription of ARGs and VFs, both of which have direct relevance to human health. Transcription of such genes has been overlooked in previous studies.

Microorganisms are useful biological indicators of toxicity and play a key role in the functioning of healthy soils. In this study, we investigated the residual toxicity of hydrocarbons in aged contaminated soils and determined the extent of microbial community recovery during in-situ bioremediation at subantarctic Macquarie Island. Previously identified microbial indicators of hydrocarbon toxicity were used to understand interactions between hydrocarbon concentrations, soil physicochemical parameters and the microbial community. Despite the complexity of the field sites, which included active fuel storage areas with high levels of soil heterogeneity, multiple spill events and variable fuel sources, we observed consistent microbial community traits associated with exposure to high concentrations of hydrocarbons. These included; reductions in alpha diversity, inhibition of nitrification potential and a reduction in the ratio of oligotrophic to copiotrophic species. These observed responses and the sensitivity of microbial communities in the field, were comparable to sensitivity estimates obtained in a previous lab-based mesocosm study with hydrocarbon spiked soils. This study provides a valuable and often missing link between the quite disparate conditions of controlled lab-based spiking experiments and the complexity presented by ‘real-world’ contaminated field sites.

Sertraline is a widely used antidepressant that becomes an aquatic pollutant through metabolic excretion and improper disposal. Determining the impact of sertraline on benthic microbial ecosystems is important for the transformation of river biogenic elements. However, the molecular initiating event induced by sertraline is more readily observed at higher levels, such as the individual or population level of larger organisms, and the effect is not pronounced in benthic organisms, which are directly involved in nitrogen transformation. Therefore, this study used DNA metabarcoding to analyze the effect of sertraline on the microbial ecosystem and material cycles in river sediment through the lens of a microbial food web. The presence of sertraline in the river sediment enhanced the mineralization capacity of nitrogen and increased the accumulation of nitrate in the sediment. Sertraline affected the structure of the microbial food web by stimulating different successions of bacteria and eukaryotes. A structural equation model revealed that sertraline affected the microbial food web model through top-down forces (predation) by reducing the trophic transfer efficiency from metazoans to protozoans. This effect resulted in decreases in the trophic transfer efficiency from protozoans to bacteria and increases in nitrogen mineralization capacity. This was followed by a gradual increase in the nitrification reaction under the action of nitrifying bacteria, increasing the threat to the ecological health of rivers. The results show that sertraline affects the material cycle of river ecosystems and emphasizes that the assessment of the ecological risks of sertraline needs to be considered from the perspective of the material cycle of ecosystems.