SUMMARY The majority of life on Earth—notably, microbial life—occurs in places that do not receive sunlight, with the habitats of the oceans being the largest of these reservoirs. Sunlight penetrates only a few tens to hundreds of meters into the ocean, resulting in large-scale microbial ecosystems that function in the dark. Our knowledge of microbial processes in the dark ocean—the aphotic pelagic ocean, sediments, oceanic crust, hydrothermal vents, etc.—has increased substantially in recent decades. Studies that try to decipher the activity of microorganisms in the dark ocean, where we cannot easily observe them, are yielding paradigm-shifting discoveries that are fundamentally changing our understanding of the role of the dark ocean in the global Earth system and its biogeochemical cycles. New generations of researchers and experimental tools have emerged, in the last decade in particular, owing to dedicated research programs to explore the dark ocean biosphere. This review focuses on our current understanding of microbiology in the dark ocean, outlining salient features of various habitats and discussing known and still unexplored types of microbial metabolism and their consequences in global biogeochemical cycling. We also focus on patterns of microbial diversity in the dark ocean and on processes and communities that are characteristic of the different habitats.
The Louisiana shelf is the largest zone of seasonally oxygen-depleted coastal bottom water in the U.S. This condition results from the high freshwater and nutrient input from the Mississippi River and the resulting high primary productivity in the river plume. The hypoxic zone has doubled in area since regular measurements began in 1985. Identification of the nutrient(s) limiting phytoplankton growth on the shelf and their sources is important for developing hypoxia-reduction strategies; nitrogen (N) has been considered the most important to date. In this study, we measured multiple parameters addressing nutrient limitation or stress (nutrient concentrations and ratios, alkaline phosphatase activity, phosphorus (P)turnover times, and changes in chlorophyll a concentrations in nutrient enrichment bioassays) in the Mississippi River plume in March, May, July, and September of 2001. All results indicate that phytoplankton growth on the Louisiana shelf was limited by P in May and July of 2001. P limitation was weakly evident in March, but N was limiting in September. The observed P limitation in spring and summer probably results from the historical increases in riverine N due to excessive N loading and has potential implications for developing hypoxia reduction strategies.
Hydrothermal chimneys are a globally dispersed habitat on the seafloor associated with mid-ocean ridge (MOR) spreading centers. Active, hot, venting sulfide structures from MORs have been examined for microbial diversity and ecology since their discovery in the mid-1970s, and recent work has also begun to explore the microbiology of inactive sulfides—structures that persist for decades to millennia and form moderate to massive deposits at and below the seafloor. Here we used tag pyrosequencing of the V6 region of the 16S rRNA and full-length 16S rRNA sequencing on inactive hydrothermal sulfide chimney samples from 9°N on the East Pacific Rise to learn their bacterial composition, metabolic potential, and succession from venting to nonventing (inactive) regimes. Alpha-, beta-, delta-, and gammaproteobacteria and members of the phylum Bacteroidetes dominate all inactive sulfides. Greater than 26% of the V6 tags obtained are closely related to lineages involved in sulfur, nitrogen, iron, and methane cycling. Epsilonproteobacteria represent <4% of the V6 tags recovered from inactive sulfides and 15% of the full-length clones, despite their high abundance in active chimneys. Members of the phylum Aquificae, which are common in active vents, were absent from both the V6 tags and full-length 16S rRNA data sets. In both analyses, the proportions of alphaproteobacteria, betaproteobacteria, and members of the phylum Bacteroidetes were greater than those found on active hydrothermal sulfides. These shifts in bacterial population structure on inactive chimneys reveal ecological succession following cessation of venting and also imply a potential shift in microbial activity and metabolic guilds on hydrothermal sulfides, the dominant biome that results from seafloor venting.
Microaerophilic, neutrophilic, iron-oxidizing bacteria (FeOB) grow via the oxidation of reduced Fe(II) at or near neutral pH, in the presence of oxygen, making them relevant in numerous environments with elevated Fe(II) concentrations. However, the biochemical mechanisms for Fe(II) oxidation by these neutrophilic FeOB are unknown, and genetic markers for this process are unavailable. In the ocean, microaerophilic microorganisms in the genus Mariprofundus of the class Zetaproteobacteria are the only organisms known to chemolithoautotrophically oxidize Fe and concurrently biomineralize it in the form of twisted stalks of iron oxyhydroxides. The aim of this study was to identify highly expressed proteins associated with the electron transport chain of microaerophilic, neutrophilic FeOB. To this end, Mariprofundus ferrooxydans PV-1 was cultivated, and its proteins were extracted, assayed for redox activity, and analyzed via liquid chromatography-tandem mass spectrometry for identification of peptides. The results indicate that a cytochrome c 4 , cbb 3 -type cytochrome oxidase subunits, and an outer membrane cytochrome c were among the most highly expressed proteins and suggest an involvement in the process of aerobic, neutrophilic bacterial Fe oxidation. Proteins associated with alternative complex III, phosphate transport, carbon fixation, and biofilm formation were abundant, consistent with the lifestyle of Mariprofundus. Iron (Fe) is one of the most abundant elements on Earth and a major component of the oceanic crust (1). The biologically catalyzed oxidation of Fe at circumneutral pH with oxygen (O 2 ) as the terminal electron acceptor has remained largely enigmatic, even though neutrophilic Fe oxidation is among the first chemoautotrophic microbial metabolisms described in the literature (2). This lack of data is due, in part, to obstacles such as culturing of fastidious microaerophilic, neutrophilic, Fe-oxidizing bacteria (FeOB); the relatively low cell densities in cultures; and the interference of Fe oxides with sample preparation. In addition to this, aerobic, neutrophilic FeOB have so far been elusive to genetic manipulation. Consequently, these challenges have impeded the ability to understand the mechanisms of neutrophilic Fe oxidation in the presence of O 2 and inhibited the development of molecular diagnostics targeting genetic markers for such a biological function (i.e., molecular probes targeting genes, transcripts, or proteins indicative of activity). Recent genomic analyses of microaerophilic, neutrophilic FeOB (3-6) have suggested genes that might be involved in Fe oxidation; however, evidence of expression of these genes in FeOB has not been shown. This is in contrast with the recent advancements in the elucidation of the mechanisms of Fe oxidation in aerobic, acidophilic bacteria (especially Acidithiobacillus ferrooxidans and Leptospirillum spp.) and neutrophilic, anoxygenic, phototrophic bacteria (Rhodopseudomonas palustris and Rhodobacter spp.) (see reference 7 for a review).Mariprofundus fer...
Eukaryotes have acquired many mechanisms to repair DNA double-strand breaks (DSBs) [1]. In the yeast Saccharomyces cerevisiae, this damage can be repaired either by homologous recombination, which depends on the Rad52 protein, or by non-homologous end-joining (NHEJ), which depends on the proteins yKu70 and yKu80 [2] [3]. How do cells choose which repair pathway to use? Deletions of the SIR2, SIR3 and SIR4 genes - which are involved in transcriptional silencing at telomeres and HM mating-type loci (HMLalpha and HMRa) in yeast [4] - have been reported to reduce NHEJ as severely as deletions of genes encoding Ku proteins [5]. Here, we report that the effect of deleting SIR genes is largely attributable to derepression of silent mating-type genes, although Sir proteins do play a minor role in end-joining. When DSBs were made on chromosomes in haploid cells that retain their mating type, sir Delta mutants reduced the frequency of NHEJ by twofold or threefold, although plasmid end-joining was not affected. In diploid cells, sir mutants showed a twofold reduction in the frequency of NHEJ in two assays. Mating type also regulated the efficiency of DSB-induced homologous recombination. In MATa/MATalpha diploid cells, a DSB induced by HO endonuclease was repaired 98% of the time by gene conversion with the homologous chromosome, whereas in diploid cells with an alpha mating type (matDelta/MATalpha) repair succeeded only 82% of the time. Mating-type regulation of genes specific to haploid or diploid cells plays a key role in determining which pathways are used to repair DSBs.
Utilization rates of inorganic and organic phosphorus by different picophytoplankton in the oligotrophic ocean are not well quantified. We used radioisotope tracers of orthophosphate (Pi) and the nucleic acid adenosine 5'triphosphate (ATP) to quantify P utilization into flow cytometrically sorted groups of picophytoplankton during the summer and fall of 2007 in the western Sargasso Sea. Dissolved organic phosphorus (DOP) dominated the dissolved P pool (mean ± SD 71 ± 56%), while soluble reactive phosphorus (SRP) concentrations were consistently < 5 nmol l -1 . All of the groups studied assimilated Pi (ρ Pi ) and ATP (ρ* ATP ) at significant rates. In addition, ρ Pi increased with ambient SRP concentrations, while ambient DOP concentrations had no apparent effect on either ρ Pi or ρ* ATP . Consistent with community composition and contributions to autotrophic biovolume, prokaryotes were primarily responsible for Pi and ATP turnover. In regions where SRP was depleted to < 3 nmol l -1 , ATP accounted for > 70% of the total P utilized. Among the individual taxa, ρ Pi and ρ* ATP increased in the order Prochlorococcus, Synechococcus, pico-, and nanoeukaryotes, when uptake was normalized to cell number, but the opposite relationship was observed when normalized to cell volume. This suggests that cyanobacteria are physiologically superior to the larger eukaryotes with respect to scavenging both Pi and ATP in the oligotrophic Sargasso Sea. A comparison of estimated C:P utilization rates with particulate C:P ratios suggests that different phytoplankton groups may be experiencing different degrees of P stress in the same ambient nutrient environment. Collectively, these data suggest that the labile DOP pool, assuming that ATP is a reasonable proxy for the labile DOP pool, in the Sargasso Sea may constrain primary productivity in the absence of sufficient SRP, and that cyanobacteria have a physiological advantage for P utilization under these conditions. KEY WORDS: Flow cytometry · Phosphate utilization · DOP utilization · Sargasso Sea · PicophytoplanktonResale or republication not permitted without written consent of the publisher Aquat Microb Ecol 58: 31-44, 2009 2001). These low concentrations have been suggested to limit microbial metabolism in the subtropical North Atlantic (Ammerman et al. 2003). Throughout most of the year in the Sargasso Sea, the majority (> 80%) of total dissolved phosphorus (TDP) exists as dissolved organic phosphorus (DOP) (Ammerman et al. 2003, M. W. Lomas et al. unpubl. data). Thus, in the absence of sufficient SRP, phytoplankton may assimilate substantial quantities of biologically labile DOP to satisfy cellular P quotas and support primary production. Indeed, Mather et al. (2008) inferred enhanced DOP utilization in the subtropical North Atlantic, relative to the subtropical South Atlantic (where SRP concentrations are 1 to 2 orders of magnitude higher), based upon significantly lower DOP concentrations and elevated alkaline phosphatase activities (APA), the enzyme that hydrolyz...
Zetaproteobacteria create extensive iron (Fe) oxide mats at marine hydrothermal vents, making them an ideal model for microbial Fe oxidation at circumneutral pH. Comparison of neutrophilic Fe oxidizer isolate genomes has revealed a hypothetical Fe oxidation pathway, featuring a homolog of the Fe oxidase Cyc2 from Acidithiobacillus ferrooxidans. However, Cyc2 function is not well verified in neutrophilic Fe oxidizers, particularly in Fe-oxidizing environments. Toward this, we analyzed genomes and metatranscriptomes of Zetaproteobacteria, using 53 new high-quality metagenome-assembled genomes reconstructed from Fe mats at Mid-Atlantic Ridge, Mariana Backarc, and Loihi Seamount (Hawaii) hydrothermal vents. Phylogenetic analysis demonstrated conservation of Cyc2 sequences among most neutrophilic Fe oxidizers, suggesting a common function. We confirmed the widespread distribution of cyc2 and other model Fe oxidation pathway genes across all represented Zetaproteobacteria lineages. High expression of these genes was observed in diverse Zetaproteobacteria under multiple environmental conditions and in incubations. The putative Fe oxidase gene cyc2 was highly expressed in situ, often as the top expressed gene. The cyc2 gene showed increased expression in Fe(II)-amended incubations, with corresponding increases in carbon fixation and central metabolism gene expression. These results substantiate the Cyc2-based Fe oxidation pathway in neutrophiles and demonstrate its significance in marine Fe-mineralizing environments. IMPORTANCE Iron oxides are important components of our soil, water supplies, and ecosystems, as they sequester nutrients, carbon, and metals. Microorganisms can form iron oxides, but it is unclear whether this is a significant mechanism in the environment. Unlike other major microbial energy metabolisms, there is no marker gene for iron oxidation, hindering our ability to track these microbes. Here, we investigate a promising possible iron oxidation gene, cyc2, in iron-rich hydrothermal vents, where iron-oxidizing microbes dominate. We pieced together diverse Zetaproteobacteria genomes, compared these genomes, and analyzed expression of cyc2 and other hypothetical iron oxidation genes. We show that cyc2 is widespread among iron oxidizers and is highly expressed and potentially regulated, making it a good marker for the capacity for iron oxidation and potentially a marker for activity. These findings will help us understand and potentially quantify the impacts of neutrophilic iron oxidizers in a wide variety of marine and terrestrial environments.
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