Multiple integrated metabolic strategies allow foraminiferan protists to thrive in anoxic marine sediments.
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ABSTRACT:
SUBMITTER: Gomaa F
PROVIDER: S-EPMC8153729 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Some of the most extreme marine habitats known are the Mediterranean deep hypersaline anoxic basins (DHABs; water depth ∼3500 m). Brines of DHABs are nearly saturated with salt, leading many to suspect they are uninhabitable for eukaryotes. While diverse bacterial and protistan communities are reported from some DHAB water-column haloclines and brines, the existence and activity of benthic DHAB protists have rarely been explored. Here, we report findings regarding protists and fungi recovered from sediments of three DHAB (Discovery, Urania, L' Atalante) haloclines, and compare these to communities from sediments underlying normoxic waters of typical Mediterranean salinity. Halocline sediments, where the redoxcline impinges the seafloor, were studied from all three DHABs. Microscopic cell counts suggested that halocline sediments supported denser protist populations than those in adjacent control sediments. Pyrosequencing analysis based on ribosomal RNA detected eukaryotic ribotypes in the halocline sediments from each of the three DHABs, most of which were fungi. Sequences affiliated with Ustilaginomycotina Basidiomycota were the most abundant eukaryotic signatures detected. Benthic communities in these DHABs appeared to differ, as expected, due to differing brine chemistries. Microscopy indicated that only a low proportion of protists appeared to bear associated putative symbionts. In a considerable number of cases, when prokaryotes were associated with a protist, DAPI staining did not reveal presence of any nuclei, suggesting that at least some protists were carcasses inhabited by prokaryotic scavengers.
| S-EPMC4233946 | biostudies-literature
Project description:The potential for oxidation of ammonia in anoxic marine sediments exists through anaerobic oxidation by Nitrosomonas-like organisms, utilizing nitrogen dioxide, coupling of nitrification, manganese reduction, and anaerobic oxidation of ammonium by planctomycetes (the Anammox process). Here we describe the presence of microbial communities with the potential to carry out these processes in a natural marine sediment system (Loch Duich, Scotland). Natural microbial communities of Planctomycetales-Verrucomicrobia and beta- and gamma-proteobacterial ammonia-oxidizing bacteria were characterized by analysis of 16S rRNA genes amplified using group-specific primers by PCR- and reverse transcription-PCR amplification of 16S rDNA and RNA, respectively. Amplification products were analyzed by sequencing of clones and by denaturant gradient gel electrophoresis (DGGE). Amplification of primers specific for Planctomycetales-Verrucomicrobia and beta-proteobacterial ammonia-oxidizing bacteria generated products at all sampling sites and depths, but no product was generated using primers specific for gamma-proteobacterial ammonia-oxidizing bacteria. 16S rDNA DGGE banding patterns indicated complex communities of beta-proteobacterial ammonia-oxidizing bacteria in anoxic marine sediments. Phylogenetic analysis of sequences from clones and those excised from DGGE gels suggests dominance of Nitrosospira cluster 1-like organisms and of strains belonging to a novel cluster represented in dominant bands in 16S rRNA DGGE banding patterns. Their presence indicates a group of organisms closely related to recognized beta-proteobacterial ammonia-oxidizing bacteria that may be selected in anoxic environments and may be capable of anoxic ammonia oxidation. Sequence analysis of planctomycete clone libraries and sequences excised from DGGE gels also demonstrated a diverse microbial community and suggested the presence of new subdivisions, but no sequence related to recognized Anammox organisms was detected.
| S-EPMC150067 | biostudies-literature
Project description:Methane (CH4) emissions from Arctic lakes are a large and growing source of greenhouse gas to the atmosphere with critical implications for global climate. Because Arctic lakes are ice covered for much of the year, understanding the metabolic flexibility of methanotrophs under anoxic conditions would aid in characterizing the mechanisms responsible for limiting CH4 emissions from high-latitude regions. Using sediments from an active CH4 seep in Lake Qalluuraq, Alaska, we conducted DNA-based stable isotope probing (SIP) in anoxic mesocosms and found that aerobic Gammaproteobacterial methanotrophs dominated in assimilating CH4. Aerobic methanotrophs were also detected down to 70 cm deep in sediments at the seep site, where anoxic conditions persist. Metagenomic analyses of the heavy DNA from 13CH4-SIP incubations showed that these aerobic methanotrophs had the capacity to generate intermediates such as methanol, formaldehyde, and formate from CH4 oxidation and to oxidize formaldehyde in the tetrahydromethanopterin (H4MPT)-dependent pathway under anoxic conditions. The high levels of Fe present in sediments, combined with Fe and CH4 profiles in the persistent CH4 seep site, suggested that oxidation of CH4, or, more specifically, its intermediates such as methanol and formaldehyde might be coupled to iron reduction. Aerobic methanotrophs also possessed genes associated with nitrogen and hydrogen metabolism, which might provide potentially alternative energy conservation options under anoxic conditions. These results expand the known metabolic spectrum of aerobic methanotrophs under anoxic conditions and necessitate the re-assessment of the mechanisms underlying CH4 oxidation in the Arctic, especially under lakes that experience extended O2 limitations during ice cover.
| S-EPMC8692461 | biostudies-literature
Project description:The oxidation of methane in anoxic marine sediments is thought to be mediated by a consortium of methane-consuming archaea and sulfate-reducing bacteria. In this study, we compared results of rRNA gene (rDNA) surveys and lipid analyses of archaea and bacteria associated with methane seep sediments from several different sites on the Californian continental margin. Two distinct archaeal lineages (ANME-1 and ANME-2), peripherally related to the order Methanosarcinales, were consistently associated with methane seep marine sediments. The same sediments contained abundant (13)C-depleted archaeal lipids, indicating that one or both of these archaeal groups are members of anaerobic methane-oxidizing consortia. (13)C-depleted lipids and the signature 16S rDNAs for these archaeal groups were absent in nearby control sediments. Concurrent surveys of bacterial rDNAs revealed a predominance of delta-proteobacteria, in particular, close relatives of Desulfosarcina variabilis. Biomarker analyses of the same sediments showed bacterial fatty acids with strong (13)C depletion that are likely products of these sulfate-reducing bacteria. Consistent with these observations, whole-cell fluorescent in situ hybridization revealed aggregations of ANME-2 archaea and sulfate-reducing Desulfosarcina and Desulfococcus species. Additionally, the presence of abundant (13)C-depleted ether lipids, presumed to be of bacterial origin but unrelated to ether lipids of members of the order Desulfosarcinales, suggests the participation of additional bacterial groups in the methane-oxidizing process. Although the Desulfosarcinales and ANME-2 consortia appear to participate in the anaerobic oxidation of methane in marine sediments, our data suggest that other bacteria and archaea are also involved in methane oxidation in these environments.
| S-EPMC92814 | biostudies-literature
Project description:Sulfate-reducing bacteria (SRB) are essential functional microbial taxa for degrading organic matter (OM) in anoxic marine environments. However, there are little experimental data regarding how SRB regulates microbial communities. Here, we applied a top-down microbial community management approach by inhibiting SRB to elucidate their contributions to the microbial community during OM degradation. Based on the highly replicated microcosms (n = 20) of five different incubation stages, we found that many microbial community properties were influenced after inhibiting SRB, including the composition, structure, network, and community assembly processes. We also found a strong coexistence pattern between SRB and other abundant phylogenetic lineages via positive frequency-dependent selection. The relative abundances of the families Synergistaceae, Peptostreptococcaceae, Dethiosulfatibacteraceae, Prolixibacteraceae, Marinilabiliaceae, and Marinifilaceae were simultaneously suppressed after inhibiting SRB during OM degradation. A close association between SRB and the order Marinilabiliales among coexisting taxa was most prominent. They contributed to preserved modules during network successions, were keystone nodes mediating the networked community, and contributed to homogeneous ecological selection. The molybdate tolerance test of the isolated strains of Marinilabiliales showed that inhibited SRB (not the inhibitor of SRB itself) triggered a decrease in the relative abundance of Marinilabiliales. We also found that inhibiting SRB resulted in reduced pH, which is unsuitable for the growth of most Marinilabiliales strains, while the addition of pH buffer (HEPES) in SRB-inhibited treatment microcosms restored the pH and the relative abundances of these bacteria. These data supported that SRB could modify niches to affect species coexistence. IMPORTANCE Our model offers insight into the ecological properties of SRB and identifies a previously undocumented dimension of OM degradation. This targeted inhibition approach could provide a novel framework for illustrating how functional microbial taxa associate the composition and structure of the microbial community, molecular ecological network, and community assembly processes. These findings emphasize the importance of SRB during OM degradation. Our results proved the feasibility of the proposed study framework, inhibiting functional taxa at the community level, for illustrating when and to what extent functional taxa can contribute to ecosystem services.
| S-EPMC10128000 | biostudies-literature
Project description:Freshwater lakes represent an important source of the potent greenhouse gas methane (CH4) to the atmosphere. Methane emissions are regulated to large parts by aerobic (MOx) and anaerobic (AOM) oxidation of methane, which are important CH4 sinks in lakes. In contrast to marine benthic environments, our knowledge about the modes of AOM and the related methanotrophic microorganisms in anoxic lake sediments is still rudimentary. Here, we demonstrate the occurrence of AOM in the anoxic sediments of Lake Sempach (Switzerland), with maximum in situ AOM rates observed within the surface sediment layers in presence of multiple groups of methanotrophic bacteria and various oxidants known to support AOM. However, substrate-amended incubations (with NO2 -, NO3 -, SO4 2-, Fe-, and Mn-oxides) revealed that none of the electron acceptors previously reported to support AOM enhanced methane turnover in Lake Sempach sediments under anoxic conditions. In contrast, the addition of oxygen to the anoxic sediments resulted in an approximately 10-fold increase in methane oxidation relative to the anoxic incubations. Phylogenetic and isotopic evidence indicate that both Type I and Type II aerobic methanotrophs were growing on methane under both oxic and anoxic conditions, although methane assimilation rates were an order of magnitude higher under oxic conditions. While the anaerobic electron acceptor responsible for AOM could not be identified, these findings expand our understanding of the metabolic versatility of canonically aerobic methanotrophs under anoxic conditions, with important implications for future investigations to identify methane oxidation processes. Bacterial AOM by facultative aerobic methane oxidizers might be of much larger environmental significance in reducing methane emissions than previously thought.
| S-EPMC9125203 | biostudies-literature
Project description:The Great Oxidation Event (GOE) was a rapid accumulation of oxygen in the atmosphere as a result of the photosynthetic activity of cyanobacteria. This accumulation reflected the pervasiveness of O2 on the planet's surface, indicating that cyanobacteria had become ecologically successful in Archean oceans. Micromolar concentrations of Fe2+ in Archean oceans would have reacted with hydrogen peroxide, a byproduct of oxygenic photosynthesis, to produce hydroxyl radicals, which cause cellular damage. Yet, cyanobacteria colonized Archean oceans extensively enough to oxygenate the atmosphere, which likely required protection mechanisms against the negative impacts of hydroxyl radical production in Fe2+ -rich seas. We identify several factors that could have acted to protect early cyanobacteria from the impacts of hydroxyl radical production and hypothesize that microbial cooperation may have played an important role in protecting cyanobacteria from Fe2+ toxicity before the GOE. We found that several strains of facultative anaerobic heterotrophic bacteria (Shewanella) with ROS defence mechanisms increase the fitness of cyanobacteria (Synechococcus) in ferruginous waters. Shewanella species with manganese transporters provided the most protection. Our results suggest that a tightly regulated response to prevent Fe2+ toxicity could have been important for the colonization of ancient ferruginous oceans, particularly in the presence of high manganese concentrations and may expand the upper bound for tolerable Fe2+ concentrations for cyanobacteria.
| S-EPMC8349797 | biostudies-literature
Project description:Anoxic riverbed sediments Raw sequence reads
| PRJNA432181 | ENA
Project description:Labyrinthulomycetes are a group of ubiquitous and diverse unicellular Stramenopiles and have long been known for their vital role in ocean carbon cycling. However, their ecological function from the perspective of organic matter degradation remains poorly understood. This study reports high-quality genomes of two newly isolated Labyrinthulomycetes strains, namely, Botryochytrium sp. strain S-28 and Oblongichytrium sp. strain S-429, and provides molecular analysis of their ecological functions using comparative genomics and a biochemical assay. Our results suggest that Labyrinthulomycetes may occupy multiple ecological niches in marine ecosystems because of the significant differences in gene function among different genera. Certain strains could degrade wheat bran independently by secreting cellulase. The key glycoside hydrolase families (GH1, GH5, and GH9) related to cellulase and the functional domains of carbohydrate-active enzymes (CAZymes) were more enriched in their genomes. This group can actively participate in marine biochemical cycles as decomposers. In contrast, other strains that could not produce cellulase may thrive as "leftover scavengers" and act as a source of nutrients to the higher-trophic-level plankton. In addition, our findings emphasize the dual roles of endoglucanase, acting as both exo- and endoglucanases, in the process of cellulose degradation. Using genomic, biochemical, and phylogenetic analyses, our study provides a broader insight into the nutritional patterns and ecological functions of Labyrinthulomycetes. IMPORTANCE Unicellular heterotrophic eukaryotes are an important component of marine ecosystems. However, their ecological functions and modes of nutrition remain largely unknown. Our current understanding of marine microbial ecology is incomplete without integrating these heterotrophic microeukaryotes into the food web models. This study focuses on the unicellular fungus-like protists Labyrinthulomycetes and provides two high-quality genomes of cellulase-producing Labyrinthulomycetes. Our study uncovers the basis of their cellulase production by deciphering the results of genomic, biochemical, and phylogenetic analyses. This study instigates a further investigation of the molecular mechanism of organic matter utilization by Labyrinthulomycetes in the world's oceans.
| S-EPMC10101102 | biostudies-literature
Project description:The purpose of present study was the simulation of an oil spill accompanied by burial of significant amount of petroleum hydrocarbons (PHs) in coastal sediments. Approximately 1000 kg of sediments collected in Messina harbor were spiked with Bunker C furnace fuel oil (6500 ppm). The rapid consumption of oxygen by aerobic heterotrophs created highly reduced conditions in the sediments with subsequent recession of biodegradation rates. As follows, after 3 months of ageing, the anaerobic sediments did not exhibit any significant levels of biodegradation and more than 80% of added Bunker C fuel oil remained buried. Anaerobic microbial community exhibited a strong enrichment in sulfate-reducing PHs-degrading and PHs-associated Deltaproteobacteria. As an effective bioremediation strategy to clean up these contaminated sediments, we applied a Modular Slurry System (MSS) allowing the containment of sediments and their physical-chemical treatment, e.g., aeration. Aeration for 3 months has increased the removal of main PHs contaminants up to 98%. As revealed by CARD-FISH, qPCR, and 16S rRNA gene clone library analyses, addition of Bunker C fuel oil initially affected the activity of autochthonous aerobic obligate marine hydrocarbonoclastic bacteria (OMHCB), and after 1 month more than the third of microbial population was represented by Alcanivorax-, Cycloclasticus-, and Marinobacter-related organisms. In the end of the experiment, the microbial community composition has returned to a status typically observed in pristine marine ecosystems with no detectable OMHCB present. Eco-toxicological bioassay revealed that the toxicity of sediments after treatment was substantially decreased. Thus, our studies demonstrated that petroleum-contaminated anaerobic marine sediments could efficiently be cleaned through an in situ oxygenation which stimulates their self-cleaning potential due to reawakening of allochtonous aerobic OMHCB.
| S-EPMC3995047 | biostudies-literature