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Rubin-Blum, M.

Publications and source records attributed to Rubin-Blum, M..

10 recordsLinked to original sources

Diverse quorum sensing systems regulate microbial communication and biogeochemical processes in deep-sea cold seeps

Quorum sensing is a fundamental chemical communication mechanism that enables microorganisms to coordinate behavior and adapt to environmental conditions. In deep-sea cold seep ecosystems, where diverse microbial communities thrive, quorum sensing is likely a key mechanism driving microbial interactions. However, the distribution, mechanisms, and ecological roles of quorum sensing in cold seeps remain poorly understood. To address this, we analyzed 173 metagenomes, 33 metatranscriptomes, and 18 metabolomes from 17 global cold seep sites. We identified 299,355 quorum sensing genes from the seep non-redundant gene catalog, representing 34 gene types across six quorum sensing systems, with distribution patterns influenced by sediment depth and seep type. These quorum sensing genes were present in 3,576 metagenome-assembled genomes from 12 archaeal and 108 bacterial phyla, revealing a complex network of intraspecies and interspecies communication. Microbial groups involved in key metabolic processes, such as sulfate-reducing bacteria, anaerobic methanotrophic archaea, diazotrophs and organohalide reducers, were extensively regulated by quorum sensing, influencing biogeochemical cycles of carbon, nitrogen, and sulfur. Phylogenetic analysis and protein domain identification highlighted the functional roles of key quorum sensing-related proteins (e.g., PDEs, CahR, RpfC/G and LuxR) in modulating microbial behaviors, such as motility and chemotaxis. Heterologous expression and metabolomic profiling further confirmed the activity of representative LuxI-R pairs and identified inhibitors of quorum sensing in cold seep sediments. Overall, these findings highlight complexity and significance of quorum sensing in microbial interactions, ecological adaptation, and biogeochemical cycling within cold seep ecosystems, advancing our understanding of microbial communication in the deep biosphere.

microbiology↗

Metabolically-versatile Ca. Thiodiazotropha symbionts of the deep-sea lucinid clam Lucinoma kazani have the genetic potential to fix nitrogen

Lucinid clams are one of the most diverse and widespread symbiont-bearing animal groups in both shallow and deep-sea chemosynthetic habitats. Lucicnids harbor Ca. Thiodiazotropha symbionts that can oxidize inorganic and organic substrates such as hydrogen sulfide and formate to gain energy. The interplay between these key metabolic functions, nutrient uptake and biotic interactions in Ca. Thiodiazotropha is not fully understood. We collected Lucinoma kazani individuals from next to a deep-sea brine pool in the eastern Mediterranean Sea, at a depth of 1150 m and used Oxford Nanopore and Illumina sequencing to obtain high-quality genomes of their Ca. Thiodiazotropha gloverae symbiont. The genomes served as the basis for transcriptomic and proteomic analyses to characterize the in situ gene expression, metabolism and physiology of the symbionts. We found genes needed for N2 fixation in the deep-sea symbionts genome, which, to date, were only found in shallow-water Ca. Thiodiazotropha. However, we did not detect the expression of these genes and thus the potential role of nitrogen fixation in this symbiosis remains to be determined. We also found the high expression of carbon fixation and sulfur oxidation genes, which indicates chemolithoautotrophy as the key physiology of Ca. Thiodiazotropha. However, we also detected the expression of pathways for using methanol and formate as energy sources. Our findings highlight the key traits these microbes maintain to support the nutrition of their hosts and interact with them.

microbiology↗

Active microbial communities facilitate carbon turnover in brine pools found in the deep Southeastern Mediterranean Sea

Discharge of gas-rich brines fuels productive chemosynthetic ecosystems in the deep sea. In these salty, methanic and sulfidic brines, microbial communities adapt to specific niches along the physicochemical gradients. However, the molecular mechanisms that underpin these adaptations are not fully known. Using metagenomics, we investigated the dense ([~]106 cell ml-1) microbial communities that occupy small deep-sea brine pools found in the Southeastern Mediterranean Sea (1150 m water depth, [~]22{degrees}C, [~]60 PSU salinity, sulfide, methane, ammonia reaching millimolar levels, and oxygen usually depleted), reaching high productivity rates of 685 {micro}g C L-1 d-1 ex-situ. We curated 266 metagenome-assembled genomes of bacteria and archaea from the several pools and adjacent sediment-water interface, highlighting the dominance of a single Sulfurimonas, which likely fuels its autotrophy using sulfide oxidation or inorganic sulfur disproportionation. This lineage may be dominant in its niche due to genome streamlining, limiting its metabolic repertoire, particularly by using a single variant of sulfide: quinone oxidoreductase. These primary producers co-exist with ANME-2c archaea that catalyze the anaerobic oxidation of methane. Other lineages can degrade the necromass aerobically (Halomonas and Alcanivorax), or anaerobically through fermentation of macromolecules (e.g., Caldatribacteriota, Bipolaricaulia, Chloroflexota, etc). These low-abundance organisms likely support the autotrophs, providing energy-rich H2, and vital organics such as vitamin B12.

microbiology↗

Tar patties are hotspots of hydrocarbon turnover and nitrogen fixation during a nearshore pollution event in the oligotrophic southeastern Mediterranean Sea

Weathered oil, that is, tar, forms hotspots of hydrocarbon degradation by complex biota in marine environment. Here, we used marker gene sequencing and metagenomics to characterize the communities of bacteria, archaea and eukaryotes that colonized tar patties and control samples (wood, plastic), collected in the littoral following an offshore spill in the warm, oligotrophic southeastern Mediterranean Sea (SEMS). We show aerobic and anaerobic hydrocarbon catabolism niches on tar interior and exterior, linking carbon, sulfur and nitrogen cycles. Alongside aromatics and larger alkanes, short-chain alkanes appear to fuel dominant populations, both the aerobic clade UBA5335 (Macondimonas), anaerobic Syntropharchaeales, and facultative Mycobacteriales. Most key organisms, including the hydrocarbon degraders and cyanobacteria, have the potential to fix dinitrogen, potentially alleviating the nitrogen limitation of hydrocarbon degradation in the SEMS. We highlight the complexity of these tar-associated communities, where bacteria, archaea and eukaryotes co-exist, exchanging metabolites and competing for resources and space. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=68 SRC="FIGDIR/small/546273v1_ufig1.gif" ALT="Figure 1"> View larger version (43K): org.highwire.dtl.DTLVardef@7ff1eborg.highwire.dtl.DTLVardef@1e39012org.highwire.dtl.DTLVardef@107c307org.highwire.dtl.DTLVardef@95073f_HPS_FORMAT_FIGEXP M_FIG C_FIG

ecology↗

Allochthonous groundwater microorganisms affect coastal seawater microbial abundance, activity and diversity

Submarine groundwater discharge (SGD) is a globally important process supplying nutrients and trace elements to the coastal environment, thus playing a pivotal role in sustaining marine primary productivity. Along with nutrients, groundwater also contains allochthonous microbes that are discharged from the terrestrial subsurface into the sea. Currently, little is known about the interactions between groundwater-borne and coastal seawater microbial populations, and their role upon introduction to coastal seawater populations. Here, we investigated seawater microbial abundance, activity and diversity in a site strongly influenced by SGD (in-situ observations), and through laboratory-controlled bottle incubations mimicking different mixing scenarios between SGD (either ambient or filtered through 0.1 {micro}m/0.22 {micro}m) and seawater. Our results demonstrate that the addition of <0.1 {micro}m SGD stimulated heterotrophic activity and increased microbial abundance compared to control, whereas <0.22 {micro}m filtration treatments induced primary productivity rates and Synechococcus growth. Amplicon sequencing of the 16S rRNA gene showed a strong shift from a SAR11-rich community in the reference SGD-unaffected coastal samples to a Rhodobacteraceae-dominated one in the <0.1 {micro}m treatment, in agreement with their in-situ enrichment in the SGD field site. These results suggest that despite the significant nutrient input, microbes delivered by SGD may affect the abundance, activity and diversity of intrinsic microbes in coastal seawater. Our results highlight the cryptic interplay between groundwater and seawater microbes in coastal environments, which has important implications for carbon cycling and climate. Key PointsO_LIGroundwater discharge into the coastal zone delivers both nutrients and allochthonous microbes. C_LIO_LIGroundwater microbes interact with seawater populations, by which affecting the delicate autotroph-heterotroph balance. C_LIO_LISubterranean microbial processes are key drivers of food webs, potentially affecting biogenic carbon fluxes in the ocean and climate. C_LI

microbiology↗

Taxonomic distribution of metabolic functions underpin nutrient cycling in Trichodesmium consortia

The photosynthetic and diazotrophic cyanobacterium Trichodesmium is a key contributor to marine biogeochemical cycles in the subtropical-oligotrophic oceans. Trichodesmium forms colonies that harbor a distinct microbial community, which expands their functional potential and is predicted to influence the cycling of carbon, nitrogen, phosphorus and iron (C, N, P, and Fe). To link key traits to taxa and elucidate how community structure influences nutrient cycling, we assessed Red Sea Trichodesmium colonies using metagenomics and metaproteomics. This diverse consortium comprises bacteria that typically associate with algae and particles, such as the ubiquitous Alteromonas macleodii, but also lineages specific to Trichodesmium, such as members from the order Balneolales. These bacteria carry functional traits that would influence resource cycling in the consortium, including siderophore biosynthesis, reduced phosphorus metabolism, vitamins, denitrification, and dissimilatory-nitrate-reduction-to-ammonium (DNRA) pathways. Denitrification and DNRA appeared to be modular as bacteria collectively completed the steps for these pathways. The vast majority of associated bacteria were auxotrophic for vitamins, indicating the interdependency of consortium members. Trichodesmium in turn may rely on associated bacteria to meet its high Fe demand as several lineages can synthesize the photolabile siderophores vibrioferrin, rhizoferrin, and petrobactin, enhancing the bioavailability of particulate-Fe to the entire consortium. Our results highlight that Trichodesmium is a hotspot for C, N, P, Fe, and vitamin exchange. The functional redundancy of nutrient cycling in the consortium likely underpins its resilience within an ever-changing global environment. ImportanceColonies of the cyanobacteria Trichodesmium act as a biological hotspot for the usage and recycling of key resources such as C, N, P and Fe within an otherwise oligotrophic environment. While Trichodesmium colonies are known to interact with a unique community of algae and particle-associated microbes, our understanding of the taxa that populate these colonies and the gene functions they encode is still limited. Characterizing the taxa and adaptive strategies that influence consortium physiology and its concomitant biogeochemistry is critical in a future ocean predicted to have increasing particulate fluxes and resource-depleted regions.

microbiology↗

Metabolic handoffs between multiple symbionts may benefit the deep-sea bathymodioline mussels

Bathymodioline mussels rely on thiotrophic and methanotrophic chemosynthetic symbionts for nutrition, yet, secondary heterotrophic symbionts are often present and play an unknown role in the fitness of the organism. The bathymodioline Idas mussels that thrive in gas seeps and on sunken wood in the Mediterranean Sea and the Atlantic Ocean, host at least six symbiont lineages that often co-occur, including the primary, chemosynthetic methane- and sulfur-oxidizing gammaproteobacteria, and the secondary Methylophagaceae, Nitrincolaceae and Flavobacteraceae symbionts, whose physiology and metabolism are obscure. Little is known about whether and how these symbionts interact or exchange metabolites. Here we curated metagenome-assembled genomes of Idas modiolaeformis symbionts and used genomecentered metatranscriptomics and metaproteomics to assess key symbiont functions. The Methylophagaceae symbiont is a methylotrophic autotroph, as it encoded and expressed the ribulose monophosphate and Calvin-Benson-Bassham cycle enzymes, particularly RuBisCO. The Nitrincolaceae ASP10-02a symbiont likely fuels its metabolism with nitrogen-rich macromolecules and may provide the holobiont with vitamin B12. The Flavobacteriaceae Urechidicola symbionts likely degrade glycans and may remove NO. Our findings indicate that these flexible associations allow for expanding the range of substrates and environmental niches, via new metabolic functions and handoffs.

microbiology↗

The worm affair: Genetic diversity in two species of symbionts that co-occur in tubeworms from the Mediterranean Sea

The symbioses between the vestimentiferan tubeworms and their chemosynthetic partners (Gammaproteobacteria, Chromatiales, Sedimenticolaceae) hallmark the success of these organisms in hydrothermal vent and hydrocarbon seep deep-sea habitats. The fidelity of these associations varies, as both the hosts and the symbionts can be loose in partner choice. Some tubeworms may host distinct symbiont phylotypes, which often co-occur in a single host individual. To better understand the genetic basis for the promiscuity of tubeworm symbioses, we curated and investigated metagenome-assembled genomes of two symbiont phylotypes (species, based on the average nucleotide identity <95%) in Lamellibrachia anaximandri, a vestimentiferan endemic to the Mediterranean Sea, in individuals collected from Palinuro hydrothermal vents (Italy) and hydrocarbon seeps (Eratosthenes seamount and Palmahim disturbance). Using comparative genomics, we show that mainly mobilome and defense mechanism-related features distinguish the symbiont genotypes. While many central metabolic functions are conserved in the tubeworm symbionts, nitrate respiration (Nar, Nap and Nas proteins) is modular, yet this modularity is not linked to speciation, but rather to local adaptation. Our results hint that variation in a single moonlighting protein may be responsible for the host-symbiont fidelity.

microbiology↗

Diversity, activity and abundance of benthic microbes in the southeastern Mediterranean Sea: A baseline for monitoring

Microbes are key players in marine sediments, yet they are not accessed routinely by monitoring programs. Here, we investigate the spatial and vertical trends in the abundance, activity and diversity of benthic archaea, bacteria and fungi of the southeastern Mediterranean Sea (SEMS), based on [~]150 samples collected by the National Monitoring Program in 2018-2020 in coastal, as well as deep-sea transects across the Israeli exclusive economic zone, using vertical profiles of short sediment cores (0-1, 1-2, 4-5, 9-10 and 19-20 cm below surface). Microbial abundance was usually low (0.01 x108 to 0.21x108 cells gr-1 sediment), while heterotrophic productivity was the highest in the nearshore stations (12{+/-}4 ng C gr-1 sediment h-1), as opposed to 0.5{+/-}0.9 ng C gr-1 sediment h-1 at the offshore sites. Using amplicon sequencing of marker genes, we identified the changes in the diversity of microbes along environmental gradients, in the four dimensions (geographic location, seabed depth, distance from the sediment surface and time). We show high taxonomic diversity of bacteria and archaea (Shannons H 5.0-6.9) and lesser diversity of fungi (Shannons H 0.2-4.8). We use DESeq2 analyses to highlight the role of ammonia-oxidizing Nitrososphaeria in the aerated sediments of the continental slope and deep bathyal plain stations and organotrophic lineages in coastal, shelf, slope, and abyssal plain sediments. Based on taxonomic diversity, we infer the metabolic potential of these communities. Analyses of fungi diversity and guilds suggest the prevalence of the saprotrophic and pathotrophic microfungi Ascomycota (70{+/-}23%) and Basidiomycota (16{+/-}18%) in the SEMS sediments. We provide a comprehensive baseline of benthic microbial populations in the SEMS and pledge for the use of microbial indices in biomonitoring of the marine environment.

microbiology↗

The hidden pangenome: comparative genomics reveals pervasive diversity in symbiotic and free-living sulfur-oxidizing bacteria

Sulfur-oxidizing Thioglobaceae, often referred to as SUP05 and Arctic96BD clades, are widespread and common to hydrothermal vents and oxygen minimum zones. They impact global biogeochemical cycles and exhibit a variety of host-associated and free-living lifestyles. The evolutionary driving forces that led to the versatility, adoption of multiple lifestyles and global success of this family are largely unknown. Here, we perform an in-depth comparative genomic analysis using all available and newly generated Thioglobaceae genomes. Gene content variation was common, throughout taxonomic ranks and lifestyles. We uncovered a pool of variable genes within most Thioglobaceae populations in single environmental samples and we referred to this as the hidden pangenome. The hidden pangenome is often overlooked in comparative genomic studies and our results indicate a much higher intra-specific diversity within environmental bacterial populations than previously thought. Our results show that core-community functions are different from species core genomes suggesting that core functions across populations are divided among the intra-specific members within a population. Defense mechanisms against foreign DNA and phages were enriched in symbiotic lineages, indicating an increased exchange of genetic material in symbioses. Our study suggests that genomic plasticity and frequent exchange of genetic material drives the global success of this family by increasing its evolvability in a heterogeneous environment.

microbiology↗