Abstract:Coastal sediments accumulate metals from anthropogenic sources and as a consequence industry is required to monitor sediment health. The total concentration of a metal does not necessarily reflect its potential toxicity or biological impact, so biological assessment tools are useful for monitoring. Rapid biological assessment tools sensitive enough to detect relatively small increases in metal concentrations would provide early warning of future ecosystem impact. The authors investigated in situ populations of… Show more
“…2). This is consistent with biogeographic surveys that have detected this group in anoxic estuarine sediments (unpublished data, accession number: JN672646), OMZs (unpublished data, accession number: MG875625), and marine sediments [79]. However, the DEV007 clade is also found in oxic seawater attached to particles [35].…”
The benthos in estuarine environments often experiences periods of regularly occurring hypoxic and anoxic conditions, dramatically impacting biogeochemical cycles. How oxygen depletion affects the growth of specific uncultivated microbial populations within these diverse benthic communities, however, remains poorly understood. Here, we applied H218O quantitative stable isotope probing (qSIP) in order to quantify the growth of diverse, uncultured bacterial populations in response to low oxygen concentrations in estuarine sediments. Over the course of 7- and 28-day incubations with redox conditions spanning from hypoxia to euxinia (sulfidic), 18O labeling of bacterial populations exhibited different patterns consistent with micro-aerophilic, anaerobic, facultative anaerobic, and aerotolerant anaerobic growth. 18O-labeled populations displaying anaerobic growth had a significantly non-random phylogenetic distribution, exhibited by numerous clades currently lacking cultured representatives within the Planctomycetes, Actinobacteria, Latescibacteria, Verrucomicrobia, and Acidobacteria. Genes encoding the beta-subunit of the dissimilatory sulfate reductase (dsrB) became 18O labeled only during euxinic conditions. Sequencing of these 18O-labeled dsrB genes showed that Acidobacteria were the dominant group of growing sulfate-reducing bacteria, highlighting their importance for sulfur cycling in estuarine sediments. Our findings provide the first experimental constraints on the redox conditions underlying increased growth in several groups of “microbial dark matter”, validating hypotheses put forth by earlier metagenomic studies.
“…2). This is consistent with biogeographic surveys that have detected this group in anoxic estuarine sediments (unpublished data, accession number: JN672646), OMZs (unpublished data, accession number: MG875625), and marine sediments [79]. However, the DEV007 clade is also found in oxic seawater attached to particles [35].…”
The benthos in estuarine environments often experiences periods of regularly occurring hypoxic and anoxic conditions, dramatically impacting biogeochemical cycles. How oxygen depletion affects the growth of specific uncultivated microbial populations within these diverse benthic communities, however, remains poorly understood. Here, we applied H218O quantitative stable isotope probing (qSIP) in order to quantify the growth of diverse, uncultured bacterial populations in response to low oxygen concentrations in estuarine sediments. Over the course of 7- and 28-day incubations with redox conditions spanning from hypoxia to euxinia (sulfidic), 18O labeling of bacterial populations exhibited different patterns consistent with micro-aerophilic, anaerobic, facultative anaerobic, and aerotolerant anaerobic growth. 18O-labeled populations displaying anaerobic growth had a significantly non-random phylogenetic distribution, exhibited by numerous clades currently lacking cultured representatives within the Planctomycetes, Actinobacteria, Latescibacteria, Verrucomicrobia, and Acidobacteria. Genes encoding the beta-subunit of the dissimilatory sulfate reductase (dsrB) became 18O labeled only during euxinic conditions. Sequencing of these 18O-labeled dsrB genes showed that Acidobacteria were the dominant group of growing sulfate-reducing bacteria, highlighting their importance for sulfur cycling in estuarine sediments. Our findings provide the first experimental constraints on the redox conditions underlying increased growth in several groups of “microbial dark matter”, validating hypotheses put forth by earlier metagenomic studies.
“…SAR324 and SAR406 are considered oligotrophic bacteria (Cho and Giovannoni, 2004), which could also explain an adaptation toward low levels of trace metal concentrations. Consistent with our findings, the Verrucomicrobia DEV007 was recently identified among the most sensitive taxa to multiple metals in a molecular screening of microbial communities for candidate indicators of multiple metal impacts performed in marine sediments from northern Australia (Cornall et al, 2016).…”
Marine microbes are an important control on the biogeochemical cycling of trace metals, but simultaneously, these metals can control the growth of microorganisms and the cycling of major nutrients like C and N. However, studies on the response/limitation of microorganisms to trace metals have traditionally focused on the response of autotrophic phytoplankton to Fe fertilization. Few reports are available on the response of heterotrophic prokaryotes to Fe, and even less to other biogeochemically relevant metals. We performed the first study coupling dark incubations with next generation sequencing to specifically target the functional and phylogenetic response of heterotrophic prokaryotes to Fe enrichment. Furthermore, we also studied their response to Co, Mn, Ni, Zn, Cu (individually and mixed), using surface and deep samples from either coastal or open-ocean waters. Heterotrophic prokaryotic activity was stimulated by Fe in surface open–ocean, as well as in coastal, and deep open-ocean waters (where Zn also stimulated). The most susceptible populations to trace metals additions were uncultured bacteria (e.g., SAR324, SAR406, NS9, and DEV007). Interestingly, hydrocarbon-degrading bacteria (e.g., Thalassolituus, Marinobacter, and Oleibacter) benefited the most from metal addition across all waters (regions/depths) revealing a predominant role in the cycling of metals and organic matter in the ocean.
“…However, we observed that the proximity to the aquaculture site was associated with the reduction of the Verrucomicrobia uncultured family DEV007 in the limpet microbiome of limpets. DEV007 is a marine group of bacteria recently pointed out as particularly sensitive to metal pollution in surface waters and marine sediments [68,69]. Its decrease in limpets growing in adhesion to the aquaculture cage might be related to the increase in heavy metal accumulation that often accompanies aquaculture practices [1], which can indirectly affect the most sensitive species in the microbiome of nearby wild organisms.…”
Aquaculture plays a major role in the coastal economy of the Mediterranean Sea. This raises the issue of the impact of fish cages on the surrounding environment. Here, we explore the impact of aquaculture on the composition of the digestive gland microbiome of a representative locally dwelling wild holobiont, the grazer gastropod Patella caerulea, at an aquaculture facility located in Southern Sicily, Italy. The microbiome was assessed in individuals collected on sea bream aquaculture cages and on a rocky coastal tract located about 1.2 km from the cages, as the control site. Patella caerulea microbiome variations were explained in the broad marine metacommunity context, assessing the water and sediment microbiome composition at both sites, and characterizing the microbiome associated with the farmed sea bream. The P. caerulea digestive gland microbiome at the aquaculture site was characterized by a lower diversity, the loss of microorganisms sensitive to heavy metal contamination, and by the acquisition of fish pathogens and parasites. However, we also observed possible adaptive responses of the P. caerulea digestive gland microbiome at the aquaculture site, including the acquisition of putative bacteria able to deal with metal and sulfide accumulation, highlighting the inherent microbiome potential to drive the host acclimation to stressful conditions.
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