Bioturbation as a key driver behind the dominance of Bacteria over Archaea in near-surface sediment.
ABSTRACT: The factors controlling the relative abundances of Archaea and Bacteria in marine sediments are poorly understood. We determined depth distributions of archaeal and bacterial 16S rRNA genes by quantitative PCR at eight stations in Aarhus Bay, Denmark. Bacterial outnumber archaeal genes 10-60-fold in uppermost sediments that are irrigated and mixed by macrofauna. This bioturbation is indicated by visual observations of sediment color and faunal tracks, by porewater profiles of dissolved inorganic carbon and sulfate, and by distributions of unsupported 210Pb and 137Cs. Below the depth of bioturbation, the relative abundances of archaeal genes increase, accounting for one third of 16S rRNA genes in the sulfate zone, and half of 16S rRNA genes in the sulfate-methane transition zone and methane zone. Phylogenetic analyses reveal a strong shift in bacterial and archaeal community structure from bioturbated sediments to underlying layers. Stable isotopic analyses on organic matter and porewater geochemical gradients suggest that macrofauna mediate bacterial dominance and affect microbial community structure in bioturbated sediment by introducing fresh organic matter and high-energy electron acceptors from overlying seawater. Below the zone of bioturbation, organic matter content and the presence of sulfate exert key influences on bacterial and archaeal abundances and overall microbial community structure.
Project description:Through a process called "bioturbation," burrowing macrofauna have altered the seafloor habitat and modified global carbon cycling since the Cambrian. However, the impact of macrofauna on the community structure of microorganisms is poorly understood. Here, we show that microbial communities across bioturbated, but geochemically and sedimentologically divergent, continental margin sites are highly similar but differ clearly from those in nonbioturbated surface and underlying subsurface sediments. Solid- and solute-phase geochemical analyses combined with modeled bioturbation activities reveal that dissolved O2 introduction by burrow ventilation is the major driver of archaeal community structure. By contrast, solid-phase reworking, which regulates the distribution of fresh, algal organic matter, is the main control of bacterial community structure. In nonbioturbated surface sediments and in subsurface sediments, bacterial and archaeal communities are more divergent between locations and appear mainly driven by site-specific differences in organic carbon sources.
Project description:Analyses of microbial diversity in marine sediments have identified a core set of taxa unique to the marine deep biosphere. Previous studies have suggested that these specialized communities are shaped by processes in the surface seabed, in particular that their assembly is associated with the transition from the bioturbated upper zone to the nonbioturbated zone below. To test this hypothesis, we performed a fine-scale analysis of the distribution and activity of microbial populations within the upper 50 cm of sediment from Aarhus Bay (Denmark). Sequencing and qPCR were combined to determine the depth distributions of bacterial and archaeal taxa (16S rRNA genes) and sulfate-reducing microorganisms (SRM) (dsrB gene). Mapping of radionuclides throughout the sediment revealed a region of intense bioturbation at 0-6 cm depth. The transition from bioturbated sediment to the subsurface below (7 cm depth) was marked by a shift from dominant surface populations to common deep biosphere taxa (e.g., Chloroflexi and Atribacteria). Changes in community composition occurred in parallel to drops in microbial activity and abundance caused by reduced energy availability below the mixed sediment surface. These results offer direct evidence for the hypothesis that deep subsurface microbial communities present in Aarhus Bay mainly assemble already centimeters below the sediment surface, below the bioturbation zone.
Project description:In marine environments, macrofauna living in or on the sediment surface may alter the structure, diversity and function of benthic microbial communities. In particular, microbial nitrogen (N)-cycling processes may be enhanced by the activity of large bioturbating organisms. Here, we study the effect of the burrowing mud shrimp Upogebia deltaura upon temporal variation in the abundance of genes representing key N-cycling functional guilds. The abundance of bacterial genes representing different N-cycling guilds displayed different temporal patterns in burrow sediments in comparison with surface sediments, suggesting that the burrow provides a unique environment where bacterial gene abundances are influenced directly by macrofaunal activity. In contrast, the abundances of archaeal ammonia oxidizers varied temporally but were not affected by bioturbation, indicating differential responses between bacterial and archaeal ammonia oxidizers to environmental physicochemical controls. This study highlights the importance of bioturbation as a control over the temporal variation in nitrogen-cycling microbial community dynamics within coastal sediments.
Project description:Ocean acidification (OA), caused by the dissolution of increasing concentrations of atmospheric carbon dioxide (CO2) in seawater, is projected to cause significant changes to marine ecology and biogeochemistry. Potential impacts on the microbially driven cycling of nitrogen are of particular concern. Specifically, under seawater pH levels approximating future OA scenarios, rates of ammonia oxidation (the rate-limiting first step of the nitrification pathway) have been shown to dramatically decrease in seawater, but not in underlying sediments. However, no prior study has considered the interactive effects of microbial ammonia oxidation and macrofaunal bioturbation activity, which can enhance nitrogen transformation rates. Using experimental mesocosms, we investigated the responses to OA of ammonia oxidizing microorganisms inhabiting surface sediments and sediments within burrow walls of the mud shrimp Upogebia deltaura. Seawater was acidified to one of four target pH values (pHT 7.90, 7.70, 7.35 and 6.80) in comparison with a control (pHT 8.10). At pHT 8.10, ammonia oxidation rates in burrow wall sediments were, on average, fivefold greater than in surface sediments. However, at all acidified pH values (pH ? 7.90), ammonia oxidation rates in burrow sediments were significantly inhibited (by 79-97%; p < 0.01), whereas rates in surface sediments were unaffected. Both bacterial and archaeal abundances increased significantly as pHT declined; by contrast, relative abundances of bacterial and archaeal ammonia oxidation (amoA) genes did not vary. This research suggests that OA could cause substantial reductions in total benthic ammonia oxidation rates in coastal bioturbated sediments, leading to corresponding changes in coupled nitrogen cycling between the benthic and pelagic realms.
Project description:The hydrothermal sediments of Guaymas Basin, an active spreading center in the Gulf of California (Mexico), are rich in porewater methane, short-chain alkanes, sulfate and sulfide, and provide a model system to explore habitat preferences of microorganisms, including sulfate-dependent, methane- and short chain alkane-oxidizing microbial communities. In this study, hot sediments (above 60°C) covered with sulfur-oxidizing microbial mats surrounding a hydrothermal mound (termed "Mat Mound") were characterized by porewater geochemistry of methane, C2-C6 short-chain alkanes, sulfate, sulfide, sulfate reduction rate measurements, in situ temperature gradients, bacterial and archaeal 16S rRNA gene clone libraries and V6 tag pyrosequencing. The most abundantly detected groups in the Mat mound sediments include anaerobic methane-oxidizing archaea of the ANME-1 lineage and its sister clade ANME-1Guaymas, the uncultured bacterial groups SEEP-SRB2 within the Deltaproteobacteria and the separately branching HotSeep-1 Group; these uncultured bacteria are candidates for sulfate-reducing alkane oxidation and for sulfate-reducing syntrophy with ANME archaea. The archaeal dataset indicates distinct habitat preferences for ANME-1, ANME-1-Guaymas, and ANME-2 archaea in Guaymas Basin hydrothermal sediments. The bacterial groups SEEP-SRB2 and HotSeep-1 co-occur with ANME-1 and ANME-1Guaymas in hydrothermally active sediments underneath microbial mats in Guaymas Basin. We propose the working hypothesis that this mixed bacterial and archaeal community catalyzes the oxidation of both methane and short-chain alkanes, and constitutes a microbial community signature that is characteristic for hydrothermal and/or cold seep sediments containing both substrates.
Project description:In deep ocean hypersaline basins, the combination of high salinity, unusual ionic composition and anoxic conditions represents significant challenges for microbial life. We used geochemical porewater characterization and DNA sequencing based taxonomic surveys to enable environmental and microbial characterization of anoxic hypersaline sediments and brines in the Orca Basin, the largest brine basin in the Gulf of Mexico. Full-length bacterial 16S rRNA gene clone libraries from hypersaline sediments and the overlying brine were dominated by the uncultured halophilic KB1 lineage, Deltaproteobacteria related to cultured sulfate-reducing halophilic genera, and specific lineages of heterotrophic Bacteroidetes. Archaeal clones were dominated by members of the halophilic methanogen genus Methanohalophilus, and the ammonia-oxidizing Marine Group I (MG-I) within the Thaumarchaeota. Illumina sequencing revealed higher phylum- and subphylum-level complexity, especially in lower-salinity sediments from the Orca Basin slope. Illumina and clone library surveys consistently detected MG-I Thaumarchaeota and halotolerant Deltaproteobacteria in the hypersaline anoxic sediments, but relative abundances of the KB1 lineage differed between the two sequencing methods. The stable isotopic composition of dissolved inorganic carbon and methane in porewater, and sulfate concentrations decreasing downcore indicated methanogenesis and sulfate reduction in the anoxic sediments. While anaerobic microbial processes likely occur at low rates near their maximal salinity thresholds in Orca Basin, long-term accumulation of reaction products leads to high methane concentrations and reducing conditions within the Orca Basin brine and sediments.
Project description:Oxygen depleted areas are widespread in the marine realm. Unlike macrofauna, meiofauna are abundant in hypoxic sediments. We studied to what extent meiofauna affect oxygen availability, sulfide removal and microbial communities. Meiofauna were extracted alive and added to intact sediments simulating abundance gradients previously reported in the area. A total of 324 porewater microprofiles were recorded over a 3-week incubation period and microbial community structure and cable bacteria densities were determined at the end of the experiment. At high abundances meiofauna activity deepened oxygen penetration by 85%, 59%, and 62% after 5, 14, and 22 days, respectively, compared to control sediment with scarce meiofauna. After 6 days, meiofauna increased the volume of oxidized, sulfide-free sediment by 68% and reduced sulfide fluxes from 8.8 to 0.4 mmol m-2 d-1. After 15 days, the difference with the control attenuated due to the presence of a cable bacteria population, which facilitated sulfides oxidation in all treatments. 16S rRNA gene analysis revealed that meiofauna affected microbial community structure (beta diversity). Thus, meiofauna bioturbation plays an important role in deepening oxygen penetration, counteracting euxinia and in structuring microbial diversity of hypoxic sediments. Co-existence with cable bacteria demonstrates neutralism interaction between these two ecosystem engineers.
Project description:Seasonal hypoxia on the Louisiana continental shelf (LCS) has grown to over 22,000 km2 with limited information available on how low oxygen effects the benthos. Benthic macrofaunal colonization and sediment biogeochemical parameters were characterized at twelve stations in waters 10 - 50 m deep along four transects spanning 320 km across the LCS hypoxic zone in the early fall of 2010 when bottom waters typically return to oxic conditions. Chemical data and sediment profile imaging (SPI) support three primary mechanistic pathways of organic matter degradation on the LCS: (i) metal oxide cycling in depositional muds, (ii) infauna-driven bioturbation delivering oxygen below the sediment-water interface, and (iii) sulfate reduction in sediments where iron oxide availability is limited. The transect nearest the Mississippi River delta had the highest concentrations of porewater and solid phase Mn and Fe with SPI images of recently deposited reddish, mixed muddy sediments suggestive of metal cycling. The deepest stations had high oxidized iron concentrations and rust colored sediments with faunal colonization that suggests sediments are oxidized via bioturbation. Many nearshore and central LCS stations had more black sediments, more disturbed clay layers, lower amounts of oxidized iron, and higher sulfate reduction rates than the deepest stations. Sediment mixing coefficients, DB , determined from chlorophyll-a concentration profiles varied between 33 and 183 cm-2 y-1. DB values were highest at the deepest stations where sediments were colonized. DB were not determined at two nearshore stations where chlorophyll-a concentrations were highly variable in surficial sediments, and on the eastern shelf where sedimentation is high. This study provides a regional view of benthic faunal colonization and sediment biogeochemistry on the LCS, describes regions with potentially different pathways of organic matter degradation, and demonstrates the importance of both bioturbation and physical mixing in processing the large amounts of organic matter in river-dominated continental shelf systems.
Project description:Methane and nitrous oxide are potent greenhouse gases (GHGs) that contribute to climate change. Coastal sediments are important GHG producers, but the contribution of macrofauna (benthic invertebrates larger than 1 mm) inhabiting them is currently unknown. Through a combination of trace gas, isotope, and molecular analyses, we studied the direct and indirect contribution of two macrofaunal groups, polychaetes and bivalves, to methane and nitrous oxide fluxes from coastal sediments. Our results indicate that macrofauna increases benthic methane efflux by a factor of up to eight, potentially accounting for an estimated 9.5% of total emissions from the Baltic Sea. Polychaetes indirectly enhance methane efflux through bioturbation, while bivalves have a direct effect on methane release. Bivalves host archaeal methanogenic symbionts carrying out preferentially hydrogenotrophic methanogenesis, as suggested by analysis of methane isotopes. Low temperatures (8?°C) also stimulate production of nitrous oxide, which is consumed by benthic denitrifying bacteria before it reaches the water column. We show that macrofauna contributes to GHG production and that the extent is dependent on lineage. Thus, macrofauna may play an important, but overlooked role in regulating GHG production and exchange in coastal sediment ecosystems.
Project description:Organic matter (OM) production and degradation is important in coastal estuaries, and OM fate is strongly influenced by the coupled interactions of bioturbation and biogeochemistry. From April to September 2013 sediment cores and a benthic observing system, Wormcam, were used to investigate the in situ relationship of biogeochemistry and macrofauna bioturbation in Cape Lookout Bight North Carolina. Wormcam imagery provided a vivid depiction of macrofauna functioning in an environment not previously observed, and affirmed the importance of fine-scale temporal observations of the benthic environment in situ. Observation of macrofauna presence and bioturbation during the summer contradicted previous studies that found this area to be azoic during methane activity and sulfide build-up. Sulfate concentrations decreased while sulfide and dissolved inorganic carbon concentrations increased during the summer. This coincided with changes in the depth and rates of bioturbation. Summer burrow depths (~0.8 cm) and rates (~0.4 cm h-1) were significantly less than spring burrow depths (~3.0 cm) and rates (~1.0 cm h-1). While sulfate reduction and OM degradation increased with temperature at a microscopic level, macroscopic OM degradation was reduced. As a result, reduced conditions dominated and a thin aerobic sediment layer, a few millimeters in thickness, was visible at the sediment surface. Decreases in macrofauna burrow depth and rates diminishes the area of influence of bioturbators, limiting bioturbation and subsequently the important ecosystem functions these organisms provide.