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Microbes transform aqueous mercury (Hg) into methylmercury (MeHg), a potent neurotoxin that accumulates in terrestrial and marine food webs, with potential impacts on human health. This process requires the gene pair hgcAB , which encodes for proteins that actuate Hg methylation, and has been well described for anoxic environments. However, recent studies report potential MeHg formation in suboxic seawater, although the microorganisms involved remain poorly understood. In this study, we conducted large-scale multi-omic analyses to search for putative microbial Hg methylators along defined redox gradients in Saanich Inlet, British Columbia, a model natural ecosystem with previously measured Hg and MeHg concentration profiles. Analysis of gene expression profiles along the redoxcline identified several putative Hg methylating microbial groups, including Calditrichaeota, SAR324 and Marinimicrobia, with the last the most active based on hgc transcription levels. Marinimicrobia hgc genes were identified from multiple publicly available marine metagenomes, consistent with a potential key role in marine Hg methylation. Computational homology modelling predicts that Marinimicrobia HgcAB proteins contain the highly conserved amino acid sites and folding structures required for functional Hg methylation. Furthermore, a number of terminal oxidases from aerobic respiratory chains were associated with several putative novel Hg methylators. Our findings thus reveal potential novel marine Hg-methylating microorganisms with a greater oxygen tolerance and broader habitat range than previously recognized.

Background Vibrios are among the most diverse and ecologically important marine bacteria, which have evolved many characteristics and lifestyles to occupy various niches. The relationship between genome features and environmental adaptation strategies is an essential part for understanding the ecological functions of vibrios in the marine system. The advent of complete genome sequencing technology has provided an important method of examining the genetic characteristics of vibrios on the genomic level. Results Two Vibrio genomes were sequenced and found to occupy many unique orthologues families which absent from the previously genes pool of the complete genomes of vibrios. Comparative genomics analysis found vibrios encompass a steady core-genome and tremendous pan-genome with substantial gene gain and horizontal gene transfer events in the evolutionary history. Evolutionary analysis based on the core-genome tree suggested that V. fischeri emerged ~ 385 million years ago, along with the occurrence of cephalopods and the flourish of fish. The relatively large genomes, the high number of 16S rRNA gene copies, and the presence of R-M systems and CRISPR system help vibrios live in various marine environments. Chitin-degrading related genes are carried in nearly all the Vibrio genomes. The number of chitinase genes in vibrios has been extremely expanded compared to which in the most recent ancestor of the genus. The chitinase A genes were estimated to have evolved along with the genus, and have undergone significant purifying selective force to conserve the ancestral state. Conclusions Vibrios have experienced extremely genome expansion events during their evolutionary history, allowing them to develop various functions to spread globally. Despite their close phylogenetic relationships, vibrios were found to have a tremendous pan-genome with a steady core-genome, which indicates the highly plastic genome of the genus. Additionally, the existence of various chitin-degrading related genes and the expansion of chitinase A in the genus demonstrate the importance of the chitin utilization for vibrios. Defensive systems in the Vibrio genomes may protect them from the invasion of external DNA. These genomic features investigated here provide a better knowledge of how the evolutionary process has forged Vibrio genomes to occupy various niches.

Background The Mariana Trench is the deepest known site in the Earth’s oceans, reaching a depth of ~ 11,000 m at the Challenger Deep. Recent studies reveal that hadal waters harbor distinctive microbial planktonic communities. However, the genetic potential of microbial communities within the hadal zone is poorly understood. Results Here, implementing both culture-dependent and culture-independent methods, we perform extensive analysis of microbial populations and their genetic potential at different depths in the Mariana Trench. Unexpectedly, we observed an abrupt increase in the abundance of hydrocarbon-degrading bacteria at depths > 10,400 m in the Challenger Deep. Indeed, the proportion of hydrocarbon-degrading bacteria at > 10,400 m is the highest observed in any natural environment on Earth. These bacteria were mainly Oleibacter , Thalassolituus , and Alcanivorax genera, all of which include species known to consume aliphatic hydrocarbons. This community shift towards hydrocarbon degraders was accompanied by increased abundance and transcription of genes involved in alkane degradation. Correspondingly, three Alcanivorax species that were isolated from 10,400 m water supplemented with hexadecane were able to efficiently degrade n -alkanes under conditions simulating the deep sea, as did a reference Oleibacter strain cultured at atmospheric pressure. Abundant n- alkanes were observed in sinking particles at 2000, 4000, and 6000 m (averaged 23.5 μg/gdw) and hadal surface sediments at depths of 10,908, 10,909, and 10,911 m (averaged 2.3 μg/gdw). The δ 2 H values of n- C 16/18 alkanes that dominated surface sediments at near 11,000-m depths ranged from − 79 to − 93‰, suggesting that these sedimentary alkanes may have been derived from an unknown heterotrophic source. Conclusions These results reveal that hydrocarbon-degrading microorganisms are present in great abundance in the deepest seawater on Earth and shed a new light on potential biological processes in this extreme environment.

Background Marine Group I (MGI) Thaumarchaeota , which play key roles in the global biogeochemical cycling of nitrogen and carbon (ammonia oxidizers), thrive in the aphotic deep sea with massive populations. Recent studies have revealed that MGI Thaumarchaeota were present in the deepest part of oceans—the hadal zone (depth > 6000 m, consisting almost entirely of trenches), with the predominant phylotype being distinct from that in the “shallower” deep sea. However, little is known about the metabolism and distribution of these ammonia oxidizers in the hadal water. Results In this study, metagenomic data were obtained from 0–10,500 m deep seawater samples from the Mariana Trench. The distribution patterns of Thaumarchaeota derived from metagenomics and 16S rRNA gene sequencing were in line with that reported in previous studies: abundance of Thaumarchaeota peaked in bathypelagic zone (depth 1000–4000 m) and the predominant clade shifted in the hadal zone. Several metagenome-assembled thaumarchaeotal genomes were recovered, including a near-complete one representing the dominant hadal phylotype of MGI. Using comparative genomics, we predict that unexpected genes involved in bioenergetics, including two distinct ATP synthase genes (predicted to be coupled with H + and Na + respectively), and genes horizontally transferred from other extremophiles, such as those encoding putative di-myo-inositol-phosphate (DIP) synthases, might significantly contribute to the success of this hadal clade under the extreme condition. We also found that hadal MGI have the genetic potential to import a far higher range of organic compounds than their shallower water counterparts. Despite this trait, hadal MDI ammonia oxidation and carbon fixation genes are highly transcribed providing evidence they are likely autotrophic, contributing to the primary production in the aphotic deep sea. Conclusions Our study reveals potentially novel adaptation mechanisms of deep-sea thaumarchaeotal clades and suggests key functions of deep-sea Thaumarchaeota in carbon and nitrogen cycling. En6fqpb_2L47ybAR2Rb-e_ Video Abstract

Summary Corals are colonized by symbiotic microorganisms that profoundly influence the animal’s health. One noted symbiont is a single‐celled alga (in the dinoflagellate family Symbiodiniaceae), which provides the coral with most of its fixed carbon. Thermal stress increases the production of reactive oxygen species (ROS) by Symbiodiniaceae during photosynthesis. ROS can both damage the algal symbiont’s photosynthetic machinery and inhibit its repair, causing a positive feedback loop for the toxic accumulation of ROS. If not scavenged by the antioxidant network, excess ROS may trigger a signaling cascade ending with the coral host and algal symbiont disassociating in a process known as bleaching. We use Exaiptasia diaphana as a model for corals and constructed a consortium comprised of E. diaphana–associated bacteria capable of neutralizing ROS. We identified six strains with high free radical scavenging (FRS) ability belonging to the families Alteromonadaceae, Rhodobacteraceae, Flavobacteriaceae and Micrococcaceae. In parallel, we established a consortium of low FRS isolates consisting of genetically related strains. Bacterial whole genome sequences were used to identify key pathways that are known to influence ROS. The field of coral microbiome engineering is in its infancy and is currently limited by a lack of definitive information about the functional roles of cnidarian microbiome members. Outlined in this manuscript is the start of a complex process to identify, evaluate, and select durable and useful candidate consortium members that may buffer the coral host against climate warming. We identified six diverse bacterial strains with high free radical scavenging (FRS) ability and six conspecific/congeneric low FRS strains with a view to including them in an inoculum to mitigate the effects of thermal stress in cnidarians.

The Earth’s oceans are a huge body of water with physicochemical properties and microbial community profiles that change with depth, which in turn influences their biogeochemical cycling potential. The differences between microbial communities and their functional potential in surface to hadopelagic water samples are only beginning to be explored. Here, we used metagenomics to investigate the microbial communities and their potential to drive biogeochemical cycling in seven different water layers down the vertical profile of the Challenger Deep (0–10,500 m) in the Mariana Trench, the deepest natural point in the Earth’s oceans. We recovered 726 metagenome-assembled genomes (MAGs) affiliated to 27 phyla. Overall, biodiversity increased in line with increased depth. In addition, the genome size of MAGs at ≥4000 m layers was slightly larger compared to those at 0–2000 m. As expected, surface waters were the main source of primary production, predominantly from Cyanobacteria. Intriguingly, microbes conducting an unusual form of nitrogen metabolism were identified in the deepest waters (>10,000 m), as demonstrated by an enrichment of genes encoding proteins involved in dissimilatory nitrate to ammonia conversion (DNRA), nitrogen fixation and urea transport. These likely facilitate the survival of ammonia-oxidizing archaea α lineage, which are typically present in environments with a high ammonia concentration. In addition, the microbial potential for oxidative phosphorylation and the glyoxylate shunt was enhanced in >10,000 m waters. This study provides novel insights into how microbial communities and their genetic potential for biogeochemical cycling differs through the Challenger deep water column, and into the unique adaptive lifestyle of microbes in the Earth’s deepest seawater.

The genus Vibrio , belonging to Gammaproteobacteria of the phylum Proteobacteria , is a genetically and ecologically diverse group of heterotrophic bacteria, that are ubiquitous in marine environments, especially in coastal areas. In particular, vibrios dominate, i.e. up to 10% of the readily culturable marine bacteria in these habitats. The distribution of Vibrio spp. is shaped by various environmental parameters, notably temperature, salinity and dissolved organic carbon. Vibrio spp. may utilize a wide range of organic carbon compounds, including chitin (this may be metabolized by most Vibrio spp.), alginic acid and agar. Many Vibrio spp. have very short replication times (as short as ~10 min), which could facilitate them developing into high biomass content albeit for relatively short durations. Although Vibrio spp. usually comprise a minor portion (typically ~1% of the total bacterioplankton in coastal waters) of the total microbial population, they have been shown to proliferate explosively in response to various nutrient pulses, e.g., organic nutrients from algae blooms and iron (Fe + ) from Saharan dust. Thus, Vibrio spp. may exert large impacts on marine organic carbon cycling especially in marginal seas. Genomics and related areas of investigation will reveal more about the molecular components and mechanisms involved in Vibrio -mediated biotransformation and remineralization processes.

Background South Pacific Gyre (SPG) is the largest and clearest gyre in the world, where the concentration of surface chlorophyll a and primary production are extremely low. Aquimarina longa SW024 T was isolated from surface water of the SPG center. To understand how this bacterium could survive in this ultra-oligotrophic oceanic environment and its function in biogeochemical cycle, we sequenced the genome of A. longa SW024 T and performed extensive genomic analyses. Methods Genomic DNA was extracted and sequenced using Illumina Hiseq 2000 and Miseq platform. Genome annotation, genomic comparison and phylogenetic analyses were performed with the use of multiple bioinformatics tools like: BLAST+ 2.2.24, Glimmer3.0, RAST server, Geneious 4.8.5, ClustalW2 and MEGA5. Physiological and morphological features were tested by bacterial culture, electron microscopy, fluorescence microscopy and exopolysaccharides extraction. Results Analysis of seven Aquimarina genomes and 30 other genomes of Flavobacteriaceae isolated from seawater showed that most of the strains had low DNA G + C contents, and Aquimarina had larger genomes than other strains. Genome comparison showed varying genomic properties among seven Aquimarina genomes, including genome sizes and gene contents, which may warrant their specific adaptive strategies. Genome of A. longa SW024 T was further compared with the genomes of two other Aquimarina species which were also isolated from the SPG and A. longa SW024 T appeared to have much more genes related to replication, recombination and repair. As a copiotroph, A. longa SW024 T is long in length, and possesses large genome size and diverse transporters. However, it has also evolved many properties to survive in the oligotrophic marine environment. This bacterium grew better on solid medium than in liquid medium, suggesting it may be liable to attach to particle surfaces in order to survive in the nutrient-limiting environment. Gliding motility and the capacity to degrade various polymers possibly allow the bacterium to grow on detritus particles and use polymeric substances as carbon and energy sources. Moreover, genes related to carbon, nitrogen, and sulfur metabolisms were identified, which showed that A. longa SW024 T might be involved in various elemental cycles. Conclusions Genomic comparison of Aquimarina genus exhibits comprehensive capabilities of the strains to adapt to diverse marine environments. The genomic characteristics of A. longa SW024 T reveal that it evolves various strategies to cope with both copiotrophic and ultra-oligotrophic marine environment, which provides a better understanding of the survival abilities of bacteria in prevalent and even extreme oceanic environments. Furthermore, carbon, nitrogen and sulfur utilization of A. longa SW024 T may represent its potential functions in the global biogeochemical cycle.

South Pacific Gyre (SPG) is the largest and clearest gyre in the world, where the concentration of surface chlorophyll a and primary production are extremely low. Aquimarina longa SW024(T) was isolated from surface water of the SPG center. To understand how this bacterium could survive in this ultra-oligotrophic oceanic environment and its function in biogeochemical cycle, we sequenced the genome of A. longa SW024(T) and performed extensive genomic analyses. Genomic DNA was extracted and sequenced using Illumina Hiseq 2000 and Miseq platform. Genome annotation, genomic comparison and phylogenetic analyses were performed with the use of multiple bioinformatics tools like: BLAST+ 2.2.24, Glimmer3.0, RAST server, Geneious 4.8.5, ClustalW2 and MEGA5. Physiological and morphological features were tested by bacterial culture, electron microscopy, fluorescence microscopy and exopolysaccharides extraction. Analysis of seven Aquimarina genomes and 30 other genomes of Flavobacteriaceae isolated from seawater showed that most of the strains had low DNA G + C contents, and Aquimarina had larger genomes than other strains. Genome comparison showed varying genomic properties among seven Aquimarina genomes, including genome sizes and gene contents, which may warrant their specific adaptive strategies. Genome of A. longa SW024(T) was further compared with the genomes of two other Aquimarina species which were also isolated from the SPG and A. longa SW024(T) appeared to have much more genes related to replication, recombination and repair. As a copiotroph, A. longa SW024(T) is long in length, and possesses large genome size and diverse transporters. However, it has also evolved many properties to survive in the oligotrophic marine environment. This bacterium grew better on solid medium than in liquid medium, suggesting it may be liable to attach to particle surfaces in order to survive in the nutrient-limiting environment. Gliding motility and the capacity to degrade various polymers possibly allow the bacterium to grow on detritus particles and use polymeric substances as carbon and energy sources. Moreover, genes related to carbon, nitrogen, and sulfur metabolisms were identified, which showed that A. longa SW024(T) might be involved in various elemental cycles. Genomic comparison of Aquimarina genus exhibits comprehensive capabilities of the strains to adapt to diverse marine environments. The genomic characteristics of A. longa SW024(T) reveal that it evolves various strategies to cope with both copiotrophic and ultra-oligotrophic marine environment, which provides a better understanding of the survival abilities of bacteria in prevalent and even extreme oceanic environments. Furthermore, carbon, nitrogen and sulfur utilization of A. longa SW024(T) may represent its potential functions in the global biogeochemical cycle.