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Giant sulfur bacteria (Beggiatoaceae) from sediments underlying the Benguela upwelling system host diverse microbiomes

ABSTRACT: Due to their lithotrophic metabolisms, morphological complexity and conspicuous appearance, members of the Beggiatoaceae have been extensively studied for more than 100 years. These bacteria are known to be primarily sulfur-oxidizing autotrophs that commonly occur in dense mats at redox interfaces. Their large size and the presence of a mucous sheath allows these cells to serve as sites of attachment for communities of other microorganisms. But little is known about their individual niche preferences and attached microbiomes, particularly in marine environments, due to a paucity of cultivars and their prevalence in habitats that are difficult to access and study. Therefore, in this study, we compare Beggiatoaceae strain composition, community composition, and geochemical profiles collected from sulfidic sediments at four marine stations off the coast of Namibia. To elucidate community members that were directly attached and enriched in both filamentous Beggiatoaceae, namely Ca. Marithioploca spp. and Ca. Maribeggiatoa spp., as well as non-filamentous Beggiatoaceae, Ca. Thiomargarita spp., the Beggiatoaceae were pooled by morphotype for community analysis. The Beggiatoaceae samples collected from a highly sulfidic site were enriched in strains of sulfur-oxidizing Campylobacterota, that may promote a more hospitable setting for the Beggiatoaceae, which are known to have a lower tolerance for high sulfide to oxygen ratios. We found just a few host-specific associations with the motile filamentous morphotypes. Conversely, we detected 123 host specific enrichments with non-motile chain forming Beggiatoaceae. Potential metabolisms of the enriched strains include fermentation of host sheath material, syntrophic exchange of H2 and acetate, inorganic sulfur metabolism, and nitrite oxidation. Surprisingly, we did not detect any enrichments of anaerobic ammonium oxidizing bacteria as previously suggested and postulate that less well-studied anaerobic ammonium oxidation pathways may be occurring instead.

SUBMITTER: Flood B

PROVIDER: S-EPMC8612568 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Abstract Despite their role in modulating the marine ecosystem, variability and drivers of low‐oxygen events in the offshore northern Benguela Upwelling System (BenUS) have been rarely investigated due to the events' episodicity which is difficult to resolve using shipboard measurements. We address this issue using 4 months of high‐resolution glider data collected between February and June 2018, 100 km offshore at 18°S. We find that oxygen (O2) concentrations in the offshore northern Benguela are determined by the subsurface alternation of low‐oxygen Angola‐derived water and oxygenated water from the south at 100–500 m depth. We observe intermittent hypoxia (O2 < 60 μmol kg−1) which occurs on average for ∼30% of the 4 months deployment and is driven by the time‐varying subsurface pulses of Angola‐derived tropical water. Hypoxic events are rather persistent at depths of 300–450 m, while they are more sporadic and have weekly duration at shallower depths (100–300 m). We find extreme values of hypoxia, with O2 minima of 16 μmol kg−1, associated with an anticyclonic eddy spinning from the undercurrent flowing on the BenUS shelf and showing no surface signature. Fine‐scale patchiness and water mass mixing are associated with cross‐frontal stirring by a large anticyclone recirculating tropical water into the northern BenUS. The dominance of physical drivers and their high variability on short time scales reveal a dynamic coupling between Angola and Benguela, calling for long‐term and high‐resolution measurements and studies focusing on future changes of both tropical O2 minima and lateral fluxes in this region. Key Points Alternating subsurface physical fluxes of Angola‐ and Benguela‐derived waters drive mesopelagic oxygen (O2) variability in the offshore Benguela Hypoxic events (O2 < 60 μmol) are intermittent and are associated with weekly pulses of tropical water in the upper mesopelagic Mesoscale eddies further modulate the O2 field and are associated with severe hypoxia, fine‐scale O2 patchiness and water mass mixing

Project description:Upwelling areas are shaped by enhanced primary production in surface waters, accompanied by a well-investigated planktonic succession. Although bacteria play an important role in biogeochemical cycles of upwelling systems, little is known about bacterial community composition and its development during upwelling events. The aim of this study was to investigate the succession of bacterial assemblages in aging upwelled water of the Benguela upwelling from coastal to offshore sites. Water from the upper mixed layer at 12 stations was sampled along two transects from the origin of the upwelling to a distance of 220 km. 16S rRNA gene amplicon sequencing was then used in a bacterial diversity analysis and major bacterial taxa were quantified by catalyzed reporter deposition-fluorescence in situ hybridization. Additionally, bacterial cell numbers and bacterial production were assessed. Community statistical analysis revealed a reproducible zonation along the two transects, with four clusters of significantly different microbial assemblages. Clustering was mainly driven by phytoplankton composition and abundance. Similar to the temporal succession that occurs during phytoplankton blooms in temperate coastal waters, operational taxonomic units (OTUs) affiliated with Bacteroidetes and Gammaproteobacteria were dominant during algal blooming whereas "Pelagibacterales" were highly abundant in regions with low algal abundance. The most dominant heterotrophic OTU (9% of all reads) was affiliated with "Pelagibacterales" and showed a strong negative correlation with phytoplankton. By contrast, the second most abundant heterotrophic OTU (6% of all reads) was affiliated with the phylum Verrucomicrobia and correlated positively with phytoplankton. Together with the close relation of bacterial production and phytoplankton abundance, our results showed that bacterial community dynamics is strongly driven by the development and composition of the phytoplankton community.

Project description:BackgroundBiofilms in sulfide-rich springs present intricate microbial communities that play pivotal roles in biogeochemical cycling. We studied chemoautotrophically based biofilms that host diverse CPR bacteria and grow in sulfide-rich springs to investigate microbial controls on biogeochemical cycling.ResultsSulfide springs biofilms were investigated using bulk geochemical analysis, genome-resolved metagenomics, and scanning transmission X-ray microscopy (STXM) at room temperature and 87 K. Chemolithotrophic sulfur-oxidizing bacteria, including Thiothrix and Beggiatoa, dominate the biofilms, which also contain CPR Gracilibacteria, Absconditabacteria, Saccharibacteria, Peregrinibacteria, Berkelbacteria, Microgenomates, and Parcubacteria. STXM imaging revealed ultra-small cells near the surfaces of filamentous bacteria that may be CPR bacterial episymbionts. STXM and NEXAFS spectroscopy at carbon K and sulfur L2,3 edges show that filamentous bacteria contain protein-encapsulated spherical elemental sulfur granules, indicating that they are sulfur oxidizers, likely Thiothrix. Berkelbacteria and Moranbacteria in the same biofilm sample are predicted to have a novel electron bifurcating group 3b [NiFe]-hydrogenase, putatively a sulfhydrogenase, potentially linked to sulfur metabolism via redox cofactors. This complex could potentially contribute to symbioses, for example, with sulfur-oxidizing bacteria such as Thiothrix that is based on cryptic sulfur cycling. One Doudnabacteria genome encodes adjacent sulfur dioxygenase and rhodanese genes that may convert thiosulfate to sulfite. We find similar conserved genomic architecture associated with CPR bacteria from other sulfur-rich subsurface ecosystems.ConclusionsOur combined metagenomic, geochemical, spectromicroscopic, and structural bioinformatics analyses of biofilms growing in sulfide-rich springs revealed consortia that contain CPR bacteria and sulfur-oxidizing Proteobacteria, including Thiothrix, and bacteria from a new family within Beggiatoales. We infer roles for CPR bacteria in sulfur and hydrogen cycling. Video Abstract.

Project description:Host microbiomes are important regulators of organismal fitness, physiology, and ecology. Microbiomes promote the fitness of their host in part by buffering the host from the full effects of fluctuating conditions and stressors imposed by the external environment. Whether the host conversely serves as a buffer for their associated microbes against variation in the external environment is less clear. Here, we test if bacteria inhabiting the microbiome of a host are locally adapted to nutrient levels in their surrounding external environment. We used a system in which the host, the phytoplankter Microcystis aeruginosa, has strains that are locally adapted to low-nutrient versus high-nutrient lakes. Assessing 40 metagenome-assembled genomes belonging to four taxonomic groups of heterotrophic bacteria residing within the host microbiome, we found consistent phylogenetic divergence between strains originating from low-nutrient versus high-nutrient environments. Bacteria found in association with low-nutrient host genotypes obtained from low-nutrient lakes demonstrated genome streamlining, including reduced genome size and fewer sigma factors. These bacterial genomes have features that would facilitate survival in low-nutrient lakes, including (i) greater number of alkaline phosphatase genes that are essential for phosphorus acquisition and (ii) positive selection within genes involved in phosphorus metabolism. Overall, our results demonstrate that despite living in close association with host organisms, bacteria residing within microbiomes may have evolved and undergone environmental selection to stressors external to their host, demonstrating similar patterns of adaptation to those that might be expected to develop among free-living bacteria. IMPORTANCE Understanding how natural selection has historically shaped the traits of microbial populations comprising host microbiomes would help predict how the functions of these microbes may continue to evolve over space and time. Numerous host-associated microbes have been found to adapt to their host, sometimes becoming obligate symbionts, whereas free-living microbes are best known to adapt to their surrounding environment. Our study assessed the selective pressures of both the host environment and the surrounding external environment in shaping the functional potential of host-associated bacteria. Despite residing within the resource-rich microbiome of their hosts, we demonstrate that host-associated heterotrophic bacteria show evidence of trait selection that matches the nutrient availability of their broader surrounding environment. These findings illustrate the complex mix of selective pressures that likely shape the present-day function of bacteria found inhabiting host microbiomes. Our study lends insight into the shifts in function that may occur as environments fluctuate over time.

Project description:We investigated the seasonal and annual variability of surface sulphur plumes in the northern Benguela upwelling system off Namibia because of their significant impacts on the marine ecosystem, fishing industry, aquaculture farming and tourism due to their toxic properties. We identified the sulphur plumes in ocean colour satellite data of the medium resolution imaging spectrometer (MERIS) for the 2002-2012 time period using the differences in the spectral properties of Namibian Benguela optical water types. The sulphur events have a strong seasonal cycle with pronounced main and off-seasons forced by local and remote-driven processes. The main peak season is in late austral summer and early austral autumn at the beginning of the annual upwelling cycle caused by increasing equatorwards alongshore winds. The sulphur plume activity is high between February and April during the seasonal oxygen minimum associated with the seasonal reduction of cross-shore ventilation of the bottom waters, the seasonal southernmost position of the Angola Benguela Frontal Zone, the seasonal maximum of water mass fractions of South Atlantic and Angola Gyre Central Waters as well as the seasonal arrival of the downwelling coastal trapped waves. The off-season is in austral spring and early austral summer during increased upwelling intensity and enhanced oxygen supply. The annual variability of sulphur events is characterized by very high activities in years 2004, 2005 and 2010 interrupted by periods of lower activity in years 2002 to 2003, 2006 to 2009 and 2011 to 2012. This result can be explained by the relative contributions or adding effects of local and remote-driven forces (from the equatorial area). The probability for the occurrence of sulphur plumes is enhanced in years with a lower annual mean of upwelling intensity, decreased oxygen supply associated with decreased lateral ventilation of bottom waters, more southern position of the Angola Benguela Frontal Zone, increased mass fraction of South Atlantic Central Water and stronger downwelling coastal trapped waves. Understanding of the variability and forcing processes of the toxic sulphur events will help in the future to monitor and forecast them as well as to manage their social and economic consequences in the northern Benguela upwelling system off Namibia.

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Giant sulfur bacteria (Beggiatoaceae) from sediments underlying the Benguela upwelling system host diverse microbiomes

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