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Journal ArticleDOI

The metagenome of the marine anammox bacterium 'Candidatus Scalindua profunda' illustrates the versatility of this globally important nitrogen cycle bacterium

TL;DR: Adaptations of Scalindua to the substrate limitation of the ocean may include highly expressed ammonium, nitrite and oligopeptide transport systems and pathways for the transport, oxidation, and assimilation of small organic compounds that may allow a more versatile lifestyle contributing to the competitive fitness of ScalIndua in the marine realm.
Abstract: Anaerobic ammonium-oxidizing (anammox) bacteria are responsible for a significant portion of the loss of fixed nitrogen from the oceans, making them important players in the global nitrogen cycle. To date, marine anammox bacteria found in marine water columns and sediments worldwide belong almost exclusively to the ‘Candidatus Scalindua’ species, but the molecular basis of their metabolism and competitive fitness is presently unknown. We applied community sequencing of a marine anammox enrichment culture dominated by ‘Candidatus Scalindua profunda’ to construct a genome assembly, which was subsequently used to analyse the most abundant gene transcripts and proteins. In the S. profunda assembly, 4756 genes were annotated, and only about half of them showed the highest identity to the only other anammox bacterium of which a metagenome assembly had been constructed so far, the freshwater ‘Candidatus Kuenenia stuttgartiensis’. In total, 2016 genes of S. profunda could not be matched to the K. stuttgartiensis metagenome assembly at all, and a similar number of genes in K. stuttgartiensis could not be found in S. profunda. Most of these genes did not have a known function but 98 expressed genes could be attributed to oligopeptide transport, amino acid metabolism, use of organic acids and electron transport. On the basis of the S. profunda metagenome, and environmental metagenome data, we observed pronounced differences in the gene organization and expression of important anammox enzymes, such as hydrazine synthase (HzsAB), nitrite reductase (NirS) and inorganic nitrogen transport proteins. Adaptations of Scalindua to the substrate limitation of the ocean may include highly expressed ammonium, nitrite and oligopeptide transport systems and pathways for the transport, oxidation, and assimilation of small organic compounds that may allow a more versatile lifestyle contributing to the competitive fitness of Scalindua in the marine realm.

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Citations
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Journal ArticleDOI
TL;DR: The simultaneous presence and activity of organoheterotrophic Denitrifying bacteria, sulfide-dependent denitrifiers, and anammox bacteria suggests a tight network of bacteria coupling carbon-, nitrogen-, and sulfur cycling in Lake Grevelingen sediments.
Abstract: Denitrifying and anammox bacteria are involved in the nitrogen cycling in marine sediments but the environmental factors that regulate the relative importance of these processes are not well constrained. Here, we evaluated the abundance, diversity, and potential activity of denitrifying, anammox, and sulfide-dependent denitrifying bacteria in the sediments of the seasonally hypoxic saline Lake Grevelingen, known to harbor an active microbial community involved in sulfur oxidation pathways. Depth distributions of 16S rRNA gene, nirS gene of denitrifying and anammox bacteria, aprA gene of sulfur-oxidizing and sulfate-reducing bacteria, and ladderane lipids of anammox bacteria were studied in sediments impacted by seasonally hypoxic bottom waters. Samples were collected down to 5 cm depth (1 cm resolution) at three different locations before (March) and during summer hypoxia (August). The abundance of denitrifying bacteria did not vary despite of differences in oxygen and sulfide availability in the sediments, whereas anammox bacteria were more abundant in the summer hypoxia but in those sediments with lower sulfide concentrations. The potential activity of denitrifying and anammox bacteria as well as of sulfur-oxidizing, including sulfide-dependent denitrifiers and sulfate-reducing bacteria, was potentially inhibited by the competition for nitrate and nitrite with cable and/or Beggiatoa-like bacteria in March and by the accumulation of sulfide in the summer hypoxia. The simultaneous presence and activity of organoheterotrophic denitrifying bacteria, sulfide-dependent denitrifiers, and anammox bacteria suggests a tight network of bacteria coupling carbon-, nitrogen-, and sulfur cycling in Lake Grevelingen sediments.

946 citations


Cites background from "The metagenome of the marine anammo..."

  • ...…study (20 sequences out of 21) were part of one cluster (cluster 1, Figure 3) closely related to nirS sequences of “Candidatus Scalindua profunda” (van de Vossenberg et al., 2013), and of uncultured bacteria obtained from continental margin sediment of the Arabian Sea (Sokoll et al., 2012) and…...

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Journal ArticleDOI
TL;DR: An analysis of the metabolic opportunities of anammox bacteria suggests alternative chemolithotrophic lifestyles that are independent of these compounds, and current concepts are still largely hypothetical and put forward the most intriguing questions that need experimental answers.
Abstract: Anaerobic ammonium-oxidizing (anammox) bacteria primarily grow by the oxidation of ammonium coupled to nitrite reduction, using CO2 as the sole carbon source. Although they were neglected for a long time, anammox bacteria are encountered in an enormous species (micro)diversity in virtually any anoxic environment that contains fixed nitrogen. It has even been estimated that about 50% of all nitrogen gas released into the atmosphere is made by these ‘impossible’ bacteria. Anammox catabolism most likely resides in a special cell organelle, the anammoxosome, which is surrounded by highly unusual ladder-like (ladderane) lipids. Ammonium oxidation and nitrite reduction proceed in a cyclic electron flow through two intermediates, hydrazine and nitric oxide, resulting in the generation of proton-motive force for ATP synthesis. Reduction reactions associated with CO2 fixation drain lectrons from this cycle, and they are replenished by the oxidation of nitrite to nitrate. Besides ammonium or nitrite, anammox bacteria use a broad range of organic and inorganic compounds as electron donors. An analysis of the metabolic opportunities even suggests alternative chemolithotrophic lifestyles that are independent of these compounds. We note that current concepts are still largely hypothetical and put forward the most intriguing questions that need experimental answers.

430 citations


Cites background from "The metagenome of the marine anammo..."

  • ...Meanwhile, the partial genome of B. fulgida was described (Gori et al., 2011), followed by the recent publication of the genome of the marine species S. profunda (Van de Vossenberg et al., 2012)....

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  • ...In the S. profunda assembly (4664 ORFs), for instance, only 693 genes had significant BLASTN hits with K. stuttgartiensis (Van de Vossenberg et al., 2012)....

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  • ...Within these biofilm aggregates, the microorganisms are associated with a variety of other very diverse species (e.g. Strous et al., 2006; Van de Vossenberg et al., 2012)....

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  • ...On the other hand, the S. profunda genome contains two putative citrate synthase genes (scal03477 and scal01583) (Van de Vossenberg et al., 2012)....

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  • ...In striking contrast, NirS is one of the most abundant proteins in S. profunda (Van de Vossenberg et al., 2012)....

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Journal ArticleDOI
TL;DR: New analytical technologies are revealing vanishingly low oxygen concentrations in nitrite-rich OMZs, indicating that these AMZs are essentially anoxic marine zones (AMZs), and previously unrecognized episodic intrusions of oxygen into the AMZ core are revealed, which could periodically support aerobic metabolisms in a typically anoxic environment.
Abstract: Vast expanses of oxygen-deficient and nitrite-rich water define the major oxygen minimum zones (OMZs) of the global ocean. They support diverse microbial communities that influence the nitrogen economy of the oceans, contributing to major losses of fixed nitrogen as dinitrogen (N2) and nitrous oxide (N2O) gases. Anaerobic microbial processes, including the two pathways of N2 production, denitrification and anaerobic ammonium oxidation, are oxygen-sensitive, with some occurring only under strictly anoxic conditions. The detection limit of the usual method (Winkler titrations) for measuring dissolved oxygen in seawater, however, is much too high to distinguish low oxygen conditions from true anoxia. However, new analytical technologies are revealing vanishingly low oxygen concentrations in nitrite-rich OMZs, indicating that these OMZs are essentially anoxic marine zones (AMZs). Autonomous monitoring platforms also reveal previously unrecognized episodic intrusions of oxygen into the AMZ core, which could periodically support aerobic metabolisms in a typically anoxic environment. Although nitrogen cycling is considered to dominate the microbial ecology and biogeochemistry of AMZs, recent environmental genomics and geochemical studies show the presence of other relevant processes, particularly those associated with the sulfur and carbon cycles. AMZs correspond to an intermediate state between two “end points” represented by fully oxic systems and fully sulfidic systems. Modern and ancient AMZs and sulfidic basins are chemically and functionally related. Global change is affecting the magnitude of biogeochemical fluxes and ocean chemical inventories, leading to shifts in AMZ chemistry and biology that are likely to continue well into the future.

369 citations


Cites background from "The metagenome of the marine anammo..."

  • ...Transcripts of these aerobic organisms, however, are essentially absent in the core of the open-ocean AMZ at 200 m, where sequences matching the anammox bacterium “Candidatus Scalindua profunda” (30) are prominent (Fig....

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Journal ArticleDOI
TL;DR: The current knowledge of anammox bacterial ecology and physiology is summarized in this review to assess the potential ecological niche partitioning ofAnammox bacteria in natural and synthetic ecosystems.
Abstract: Summary Anaerobic ammonium oxidation (anammox) is a microbial process in which NH4+ is oxidized to N2 gas with NO2− as an electron acceptor. The anammox process is mediated by bacterial members affiliated with the phylum Planctomycetes, which are ubiquitously detected from anoxic natural and man-made ecosystems and a key player in the global nitrogen cycle. In the past two decades, phylogenetically different anammox bacteria have been recognized in natural and synthetic ecosystems (i.e. ‘Candidatus Kuenenia’, ‘Candidatus Brocadia’, ‘Candidatus Jettenia’, ‘Candidatus Anammoxoglobus’ and ‘Candidatus Scalindua’ genera), and the geographic distributions of these anammox bacteria indicate that they have genus-specific or species-specific habitats. Recently, we revealed the physiological characteristics of ‘Ca. Jettenia’ in addition to ‘Ca. Kuenenia’, ‘Ca. Brocadia’ and ‘Ca. Scalindua’, and, as a result, it is possible to compare the physiological characteristics of the anammox bacteria and discuss their niche partitioning. Therefore, we summarize the current knowledge of anammox bacterial ecology and physiology in this review to assess the potential ecological niche partitioning of anammox bacteria in natural and synthetic ecosystems.

284 citations


Cites background from "The metagenome of the marine anammo..."

  • ...…and John Wiley & Sons Ltd, Environmental Microbiology ‘Ca. Kuenenia’ (Strous et al., 2006; Speth et al., 2012), ‘Ca. Brocadia’ (Gori et al., 2011; Oshiki et al., 2015), ‘Ca. Jettenia’ (Hira et al., 2012; Hu et al., 2012b) and ‘Ca. Scalindua’ (van de Vossenberg et al., 2013; Speth et al., 2015)....

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  • ...Genes responsible for the TCA cycle are also species specific, and a complete gene set, including citrate synthase and citrate lyase, was only found in the ‘Ca. Scalindua profunda’ and ‘Ca. Scalindua brodae’ genomes (van de Vossenberg et al., 2013; Speth et al., 2015)....

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Journal ArticleDOI
TL;DR: This review presents examples of the diverse architecture, either elucidated or anticipated, and the high degree of modularity of the corresponding respiratory electron transport processes found in Bacteria and Archaea, and relates these to their respective bioenergetic mechanisms of proton motive force generation.

269 citations

References
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Journal ArticleDOI
TL;DR: The sensitivity of the commonly used progressive multiple sequence alignment method has been greatly improved and modifications are incorporated into a new program, CLUSTAL W, which is freely available.
Abstract: The sensitivity of the commonly used progressive multiple sequence alignment method has been greatly improved for the alignment of divergent protein sequences. Firstly, individual weights are assigned to each sequence in a partial alignment in order to down-weight near-duplicate sequences and up-weight the most divergent ones. Secondly, amino acid substitution matrices are varied at different alignment stages according to the divergence of the sequences to be aligned. Thirdly, residue-specific gap penalties and locally reduced gap penalties in hydrophilic regions encourage new gaps in potential loop regions rather than regular secondary structure. Fourthly, positions in early alignments where gaps have been opened receive locally reduced gap penalties to encourage the opening up of new gaps at these positions. These modifications are incorporated into a new program, CLUSTAL W which is freely available.

63,427 citations


"The metagenome of the marine anammo..." refers methods in this paper

  • ..., 2005), CLUSTALW (Thompson et al., 1994) and Muscle (Edgar, 2004)....

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  • ...Alignments of proteins were done with ProbCons (Do et al., 2005), CLUSTALW (Thompson et al., 1994) and Muscle (Edgar, 2004)....

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Journal ArticleDOI
TL;DR: MUSCLE is a new computer program for creating multiple alignments of protein sequences that includes fast distance estimation using kmer counting, progressive alignment using a new profile function the authors call the log-expectation score, and refinement using tree-dependent restricted partitioning.
Abstract: We describe MUSCLE, a new computer program for creating multiple alignments of protein sequences. Elements of the algorithm include fast distance estimation using kmer counting, progressive alignment using a new profile function we call the logexpectation score, and refinement using treedependent restricted partitioning. The speed and accuracy of MUSCLE are compared with T-Coffee, MAFFT and CLUSTALW on four test sets of reference alignments: BAliBASE, SABmark, SMART and a new benchmark, PREFAB. MUSCLE achieves the highest, or joint highest, rank in accuracy on each of these sets. Without refinement, MUSCLE achieves average accuracy statistically indistinguishable from T-Coffee and MAFFT, and is the fastest of the tested methods for large numbers of sequences, aligning 5000 sequences of average length 350 in 7 min on a current desktop computer. The MUSCLE program, source code and PREFAB test data are freely available at http://www.drive5. com/muscle.

37,524 citations


"The metagenome of the marine anammo..." refers methods in this paper

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Journal ArticleDOI
TL;DR: A fully automated service for annotating bacterial and archaeal genomes that identifies protein-encoding, rRNA and tRNA genes, assigns functions to the genes, predicts which subsystems are represented in the genome, uses this information to reconstruct the metabolic network and makes the output easily downloadable for the user.
Abstract: The number of prokaryotic genome sequences becoming available is growing steadily and is growing faster than our ability to accurately annotate them. We describe a fully automated service for annotating bacterial and archaeal genomes. The service identifies protein-encoding, rRNA and tRNA genes, assigns functions to the genes, predicts which subsystems are represented in the genome, uses this information to reconstruct the metabolic network and makes the output easily downloadable for the user. In addition, the annotated genome can be browsed in an environment that supports comparative analysis with the annotated genomes maintained in the SEED environment. The service normally makes the annotated genome available within 12–24 hours of submission, but ultimately the quality of such a service will be judged in terms of accuracy, consistency, and completeness of the produced annotations. We summarize our attempts to address these issues and discuss plans for incrementally enhancing the service. By providing accurate, rapid annotation freely to the community we have created an important community resource. The service has now been utilized by over 120 external users annotating over 350 distinct genomes.

9,397 citations


"The metagenome of the marine anammo..." refers methods in this paper

  • ...Data obtained by additional metagenome sequencing and de novo assemblies with different programs and parameters, and automated annotated with RAST (Aziz et al., 2008), were used to confirm gene sequences and lengths....

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Journal ArticleDOI
TL;DR: The ARB program package comprises a variety of directly interacting software tools for sequence database maintenance and analysis which are controlled by a common graphical user interface.
Abstract: The ARB (from Latin arbor, tree) project was initiated almost 10 years ago. The ARB program package comprises a variety of directly interacting software tools for sequence database maintenance and analysis which are controlled by a common graphical user interface. Although it was initially designed for ribosomal RNA data, it can be used for any nucleic and amino acid sequence data as well. A central database contains processed (aligned) primary structure data. Any additional descriptive data can be stored in database fields assigned to the individual sequences or linked via local or worldwide networks. A phylogenetic tree visualized in the main window can be used for data access and visualization. The package comprises additional tools for data import and export, sequence alignment, primary and secondary structure editing, profile and filter calculation, phylogenetic analyses, specific hybridization probe design and evaluation and other components for data analysis. Currently, the package is used by numerous working groups worldwide.

6,757 citations


"The metagenome of the marine anammo..." refers methods in this paper

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Journal ArticleDOI
TL;DR: Improvements of the currently most popular method for prediction of classically secreted proteins, SignalP, which consists of two different predictors based on neural network and hidden Markov model algorithms, where both components have been updated.

6,492 citations


"The metagenome of the marine anammo..." refers methods in this paper

  • ...The S. profunda genome has four genes encoding transporter proteins from the Formate/Nitrite Transporter (FNT) family (Saier Jr et al., 1999), FocA/NirC, with six predicted membrane spanning helices, but no apparent predicted signal peptide (SignalP)....

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  • ...Signal peptides were predicted with SignalP (Bendtsen et al., 2004), transmembrane helices with TMHMM (Sonnhammer et al., 1998)....

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