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Environmental Microbiology Reports (2015) 7(1), 23–25
doi:10.1111/1758-2229.12229
Fortunate those that are starting now
Cornelia U. Welte and Mike S.M. Jetten, Soehngen Institute of Anaerobic Microbiology, Radboud University, Nijmegen, The Netherlands. Over the past months, we have visited several workshops to train ourselves and co-workers, visited conferences to update our knowledge and heard several amazing and awesome metagenomics presentations. The pace at which mostly our American colleagues are pushing this part of environmental microbiology forward is astonishing and deserves our deepest appreciation (e.g. Sharon and Banfield, 2013; Wrighton et al., 2014). Even with our speed read and other abilities, we can hardly keep up. The metagenomic surveys spit out nearly complete genomes of new phyla with no cultivated representatives every other day, and educated guesses have to predict their (prominent) role and contribution in the environment. In the past years, our group has subsequently invested heavily in proteomics equipment and analysis, commercial bioinformatics software and hardware, affordable next generation technology (i.e. ion torrent) and extending the metagenomics network internationally. Just after a few years, the proteomics technology is up for a severe upgrade, and the others may have to follow (too) soon, putting a strain even on our considerable resources. Despite these huge investments and efforts, we think it will not be the main technology or resources that will complete our holy grail quest of new chemolithoautotrophs; instead, we need new sophisticated bioreactor technology, defined co-cultures, single cell methods and foremost all-round and well-trained microbiologist that are able to communicate with various complementary other disciplines. For the past 20 years, our team has been pursuing the discovery of so called impossible microorganisms that can oxidize methane and ammonium without oxygen. The discovery and subsequent resolution of their molecular secrets have made the anammox bacteria a showcase example of international complementary collaborative research (Kartal et al., 2013). At the basis of this success was Marc Strous’ Delft engineering-inspired implementation of the sequencing batch reactor (SBR) technology (now cited more than 1000 times) to cultivate sufficient amounts of anammox cells for both the fundamental and applied aspects of our work (Strous et al., 1998). After years of trial and error, the SBR could be replaced by membrane bioreactors in which anammox bacteria grow © 2015 Society for Applied Microbiology and John Wiley & Sons Ltd
in suspensions of single cells (Kartal et al., 2011). In this way, even more cells of very high quality and activity could be produced to form the basis of our protein (Maalcke et al., 2014), cell biology (van Niftrik and Jetten, 2012) and molecular (Kartal et al., 2011) work that showed that hydrazine production by hydrazine synthase and hydrazine oxidation by hydrazine dehydrogenase occurs inside a specialized organelle called the anammoxosome. In the near future, the isolation of this organelle and subsequently resolving all the proteins and protein complexes will be a main target to make a beginning in the understanding of energy conservation and electron transport processes in anammox bacteria. After the first genome of an anammox bacterium was resolved in 2006 (Strous et al., 2006), many more have followed. All the anammox genomes encode a core of multiheme proteins for hydrazine and ammonium conversion. The most intriguing difference among anammox bacteria is how they convert nitrite into nitric oxide. The marine Scalindua bacteria seem to use iron-based cd1 NirS nitrite reductase, KSU1/Jettenia bacteria rely on copper-based NirK while Brocadia/Kuenenia may employ an entirely different protein that still has to be identified. For their substrates ammonium and nitrite, anammox bacteria have to rely on other processes. So far, we have investigated the cooperation of anammox bacteria with ammoniumoxidizing bacteria and archaea (Yan et al., 2012), and with sulfide-oxidizing partial denitrifiers (Russ et al., 2014). In the future, many more interactions, i.e. the competition with nitrite oxidizing bacteria, heterotrophic denitrifiers or the cooperation with dissimilatory nitrate reduction to ammonium will have to be investigated preferably with very defined co-cultures of which the genomes have been resolved. In this, the competitive fitness and potential contribution of anammox bacteria to the nitrogen cycle can be understood much better. More recently, we have put our efforts on the discovery of various microorganisms catalysing the anaerobic oxidation of methane (AOM). Using the well-proven SBR technology, freshwater sediments high in methane and nitrate were used as inoculum and ultimately resulted in the enrichment of co-cultures of archaea and bacteria (Raghoebarsing et al., 2006). Increasing nitrite concentrations resulted in a dominance of Methylomirabilis oxyfera (Ettwig et al., 2008) and enough cells to unravel some molecular secrets indicating that NO may be dismutated to supply molecular oxygen for aerobic methane activation
24 Crystal ball by this strictly anaerobic bacterium. Increasing nitrate concentrations, on the other hand, resulted in an increase of the archaeal population. These archaea have recently been described (Haroon et al., 2013) and were named Methanoperedens nitroreducens. The (meta)genome of these methanotrophs encoded a full reverse methanogenesis pathway, genes for the extracellular nitrate reductase NarG and many genes encoding c-type cytochromes. Although the metagenome does not tell us what they do, it is clearly a characteristic feature of these anaerobic methanotrophs: within the closely related methanogens, only the Methanosarcinales contain c-type cytochromes at all – for most of which we don’t know what they do – but they only encode a couple in their genomes whereas in the Methanoperedens metagenome we find more than 70. It is easy and straightforward to correlate this to the potential of nitrate reduction in Methanoperedens – the more challenging task will be the subsequent analysis of the proteins to assign a physiological function to them. For the conversion of oxidized nitrogen all the way to dinitrogen gas, AOM microorganisms may have to form stable co-cultures. So far the cooperation of AOM archaea with Methylomirabilis or anammox bacteria have been studied (Haroon et al., 2013) but more options are conceivable and have to be investigated with defined genome-based co-cultures. In this way, the competitive fitness and potential contribution of AOM to methane mitigation may be much better understood. Recently, we have started a new research line in which we want study the interactions of (an)aerobic microorganism with (wetland) plants and animals. These wetland eukaryotes may provide the microbes with ideal niches in which abundant methane and ammonium may prevail in the presences of several electron acceptors. So far we have focused on Sphagnum mosses that form a symbiosis with endo- or epiphytic methanotrophs (Raghoebarsing et al., 2005; Kip et al., 2010). The plants provide oxygen to the bacteria to oxidize methane to carbon dioxide which is returned as additional CO2 for the carbon-deprived plants. As most of the peat ecosystems are very nutrient limited, a third nitrogen-fixing party may have to enter the symbiosis (Larmola et al., 2014). Resolving the microbiomes and their functions will need effective plant microbe separation protocols, or very efficient single cell sorting and genomics to find out who is contributing or exchanging what with each other. Another focus of microbe–eukaryote interactions we are studying is the contribution of gut microbes to the degradation of dietary toxins in insects, namely root fly larvae. These insect larvae reduce the yield of crucifer crops (rapeseed, cabbages) by up to 50% and are thus a serious risk to our biofuel and food industry. The key to their success is the detoxification of plant-derived secondary metabolites that repel generalist insects. Elucidating microbial breakdown
pathways by analysing the insect gut metagenome combined with investigating the respective enzyme pathways biochemically paves the way for a thorough understanding of this mode of microbe–insect relationship. With over one million insects species on our planet, we need to learn more about the contribution of microbes to the wellbeing and lifestyle of insects (Thompson and Brune, 2013), far beyond the few insect model systems that are investigated today. Looking into the crystal ball, we predict that knowledgeable biochemists and bio-informaticians will need to work hand in hand to understand each other’s trades and integrate it into a novel metagenome-driven but biochemically and physiologically validated microbial ecology. As the microbial world proves to be increasingly complex and diverse, the use of 16S rRNA genes and other phylogenetic marker will still be important for cataloguing our environment but will become less important in predicting physiological functions. They will instead be replaced by the analysis of full genome sequences that are more easily available with current and future techniques and that comprise more valuable and reliable information. Only if we know all microbial species on our planet, the phylomarker– microbial function relationship will become valid, and we are still a far way off. The knowledge from metagenomes needs to be taken one step further, to enrich and co-cultivate microbes and test the hypotheses deducted from the genome information. Ten years ago, we could only look at biogeochemical profiles – which are still astonishingly useful! – but today we can get a glimpse into nearly full genome sequences to adjust and improve our enrichment conditions. We need to train the new generation of microbiologists accordingly, not limiting ourselves to one specialization in both research and teaching of students. Establishing new master of science programmes and graduate schools targeting (meta)genomics, biochemistry and microbial physiology skills will be instrumental in this quest to broaden the microbial ecology horizon. Thus we are very fortunate that the Netherlands Government and Radboud University has affirmed the importance of microbiology by granting a so-called gravitation programme to establish the Soehngen Institute of Anaerobic Microbiology and a research master microbiology. In this way, we will be able to facilitate the education of this new generation of microbiologists. Special attention will also be paid to gender equality and leadership training to be able to continue the strong and leading school of Dutch Microbiology that will undoubtedly unravel many more exciting secrets of our fascinating newly discovered anaerobic microorganism. Gelukkig zij die nu beginnen! Fortunate those that are starting now! (Beijerinck) www.ru.nl/masters/microbiology www.ru.nl/microbiology
© 2015 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology Reports, 7, 23–25
Crystal ball
References Ettwig, K.F., Shima, S., van de Pas-Schoonen, K.T., Kahnt, J., Medema, M.H., Op den Camp, H.J., et al. (2008) Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ Microbiol 10: 3164–3173. Haroon, M.F., Hu, S., Shi, Y., Imelfort, M., Keller, J., Hugenholtz, P., et al. (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500: 567–570. Kartal, B., Geerts, W., and Jetten, M.S. (2011) Cultivation, detection, and ecophysiology of anaerobic ammoniumoxidizing bacteria. Methods Enzymol 486: 89–108. Kartal, B., de Almeida, N.M., Maalcke, W.J., Op den Camp, H.J., Jetten, M.S., and Keltjens, J.T. (2013) How to make a living from anaerobic ammonium oxidation. FEMS Microbiol Rev 37: 428–461. Kip, N., van Winden, J.F., Pan, Y., Bodrossy, L., Reichart, G.J., Smolders, A.J.P., et al. (2010) Global prevalence of methane oxidation by symbiotic bacteria in peat-moss ecosystems. Nat Geosci 3: 617–621. Larmola, T., Leppanen, S.M., Tuittila, E.S., Aarva, M., Merila, P., Fritze, H., and Tiirola, M. (2014) Methanotrophy induces nitrogen fixation during peatland development. Proc Natl Acad Sci USA 111: 734–739. Maalcke, W.J., Dietl, A., Marritt, S.J., Butt, J.N., Jetten, M.S., Keltjens, J.T., et al. (2014) Structural basis of biological NO generation by octaheme oxidoreductases. J Biol Chem 289: 1228–1242.
25
van Niftrik, L., and Jetten, M.S. (2012) Anaerobic ammoniumoxidizing bacteria: unique microorganisms with exceptional properties. Microbiol Mol Biol Rev 76: 585–596. Raghoebarsing, A.A., Smolders, A.J., Schmid, M.C., Rijpstra, W.I., Wolters-Arts, M., Derksen, J., et al. (2005) Methanotrophic symbionts provide carbon for photosynthesis in peat bogs. Nature 436: 1153–1156. Raghoebarsing, A.A., Pol, A., van de Pas-Schoonen, K.T., Smolders, A.J., Ettwig, K.F., Rijpstra, W.I., et al. (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440: 918–921. Russ, L., Speth, D.R., Jetten, M.S., Op den Camp, H.J., and Kartal, B. (2014) Interactions between anaerobic ammonium and sulfur-oxidizing bacteria in a laboratory scale model system. Environ Microbiol [Epub ahead of print]. doi:10.1111/1462-2920.12487. Sharon, I., and Banfield, J.F. (2013) Microbiology. Genomes from metagenomics. Science 342: 1057–1058. Strous, M., Heijnen, J.J., Kuenen, J.G., and Jetten, M.S.M. (1998) The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol 50: 589–596. Strous, M., Pelletier, E., Mangenot, S., Rattei, T., Lehner, A., Taylor, M.W., et al. (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440: 790–794. Thompson, C.L., and Brune, A. (2013) Crystal ball. Environ Microbiol Rep 5: 1–16. Wrighton, K.C., Castelle, C.J., Wilkins, M.J., Hug, L.A., Sharon, I., Thomas, B.C., et al. (2014) Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer. ISME J 8: 1452–1463. Yan, J., Haaijer, S.C., Op den Camp, H.J., van Niftrik, L., Stahl, D.A., Konneke, M., et al. (2012) Mimicking the oxygen minimum zones: stimulating interaction of aerobic archaeal and anaerobic bacterial ammonia oxidizers in a laboratory-scale model system. Environ Microbiol 14: 3146–3158.
© 2015 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology Reports, 7, 23–25
Environmental Microbiology Reports (2015) 7(1), 23–25
doi:10.1111/1758-2229.12229
Fortunate those that are starting now
Cornelia U. Welte and Mike S.M. Jetten, Soehngen Institute of Anaerobic Microbiology, Radboud University, Nijmegen, The Netherlands. Over the past months, we have visited several workshops to train ourselves and co-workers, visited conferences to update our knowledge and heard several amazing and awesome metagenomics presentations. The pace at which mostly our American colleagues are pushing this part of environmental microbiology forward is astonishing and deserves our deepest appreciation (e.g. Sharon and Banfield, 2013; Wrighton et al., 2014). Even with our speed read and other abilities, we can hardly keep up. The metagenomic surveys spit out nearly complete genomes of new phyla with no cultivated representatives every other day, and educated guesses have to predict their (prominent) role and contribution in the environment. In the past years, our group has subsequently invested heavily in proteomics equipment and analysis, commercial bioinformatics software and hardware, affordable next generation technology (i.e. ion torrent) and extending the metagenomics network internationally. Just after a few years, the proteomics technology is up for a severe upgrade, and the others may have to follow (too) soon, putting a strain even on our considerable resources. Despite these huge investments and efforts, we think it will not be the main technology or resources that will complete our holy grail quest of new chemolithoautotrophs; instead, we need new sophisticated bioreactor technology, defined co-cultures, single cell methods and foremost all-round and well-trained microbiologist that are able to communicate with various complementary other disciplines. For the past 20 years, our team has been pursuing the discovery of so called impossible microorganisms that can oxidize methane and ammonium without oxygen. The discovery and subsequent resolution of their molecular secrets have made the anammox bacteria a showcase example of international complementary collaborative research (Kartal et al., 2013). At the basis of this success was Marc Strous’ Delft engineering-inspired implementation of the sequencing batch reactor (SBR) technology (now cited more than 1000 times) to cultivate sufficient amounts of anammox cells for both the fundamental and applied aspects of our work (Strous et al., 1998). After years of trial and error, the SBR could be replaced by membrane bioreactors in which anammox bacteria grow © 2015 Society for Applied Microbiology and John Wiley & Sons Ltd
in suspensions of single cells (Kartal et al., 2011). In this way, even more cells of very high quality and activity could be produced to form the basis of our protein (Maalcke et al., 2014), cell biology (van Niftrik and Jetten, 2012) and molecular (Kartal et al., 2011) work that showed that hydrazine production by hydrazine synthase and hydrazine oxidation by hydrazine dehydrogenase occurs inside a specialized organelle called the anammoxosome. In the near future, the isolation of this organelle and subsequently resolving all the proteins and protein complexes will be a main target to make a beginning in the understanding of energy conservation and electron transport processes in anammox bacteria. After the first genome of an anammox bacterium was resolved in 2006 (Strous et al., 2006), many more have followed. All the anammox genomes encode a core of multiheme proteins for hydrazine and ammonium conversion. The most intriguing difference among anammox bacteria is how they convert nitrite into nitric oxide. The marine Scalindua bacteria seem to use iron-based cd1 NirS nitrite reductase, KSU1/Jettenia bacteria rely on copper-based NirK while Brocadia/Kuenenia may employ an entirely different protein that still has to be identified. For their substrates ammonium and nitrite, anammox bacteria have to rely on other processes. So far, we have investigated the cooperation of anammox bacteria with ammoniumoxidizing bacteria and archaea (Yan et al., 2012), and with sulfide-oxidizing partial denitrifiers (Russ et al., 2014). In the future, many more interactions, i.e. the competition with nitrite oxidizing bacteria, heterotrophic denitrifiers or the cooperation with dissimilatory nitrate reduction to ammonium will have to be investigated preferably with very defined co-cultures of which the genomes have been resolved. In this, the competitive fitness and potential contribution of anammox bacteria to the nitrogen cycle can be understood much better. More recently, we have put our efforts on the discovery of various microorganisms catalysing the anaerobic oxidation of methane (AOM). Using the well-proven SBR technology, freshwater sediments high in methane and nitrate were used as inoculum and ultimately resulted in the enrichment of co-cultures of archaea and bacteria (Raghoebarsing et al., 2006). Increasing nitrite concentrations resulted in a dominance of Methylomirabilis oxyfera (Ettwig et al., 2008) and enough cells to unravel some molecular secrets indicating that NO may be dismutated to supply molecular oxygen for aerobic methane activation
24 Crystal ball by this strictly anaerobic bacterium. Increasing nitrate concentrations, on the other hand, resulted in an increase of the archaeal population. These archaea have recently been described (Haroon et al., 2013) and were named Methanoperedens nitroreducens. The (meta)genome of these methanotrophs encoded a full reverse methanogenesis pathway, genes for the extracellular nitrate reductase NarG and many genes encoding c-type cytochromes. Although the metagenome does not tell us what they do, it is clearly a characteristic feature of these anaerobic methanotrophs: within the closely related methanogens, only the Methanosarcinales contain c-type cytochromes at all – for most of which we don’t know what they do – but they only encode a couple in their genomes whereas in the Methanoperedens metagenome we find more than 70. It is easy and straightforward to correlate this to the potential of nitrate reduction in Methanoperedens – the more challenging task will be the subsequent analysis of the proteins to assign a physiological function to them. For the conversion of oxidized nitrogen all the way to dinitrogen gas, AOM microorganisms may have to form stable co-cultures. So far the cooperation of AOM archaea with Methylomirabilis or anammox bacteria have been studied (Haroon et al., 2013) but more options are conceivable and have to be investigated with defined genome-based co-cultures. In this way, the competitive fitness and potential contribution of AOM to methane mitigation may be much better understood. Recently, we have started a new research line in which we want study the interactions of (an)aerobic microorganism with (wetland) plants and animals. These wetland eukaryotes may provide the microbes with ideal niches in which abundant methane and ammonium may prevail in the presences of several electron acceptors. So far we have focused on Sphagnum mosses that form a symbiosis with endo- or epiphytic methanotrophs (Raghoebarsing et al., 2005; Kip et al., 2010). The plants provide oxygen to the bacteria to oxidize methane to carbon dioxide which is returned as additional CO2 for the carbon-deprived plants. As most of the peat ecosystems are very nutrient limited, a third nitrogen-fixing party may have to enter the symbiosis (Larmola et al., 2014). Resolving the microbiomes and their functions will need effective plant microbe separation protocols, or very efficient single cell sorting and genomics to find out who is contributing or exchanging what with each other. Another focus of microbe–eukaryote interactions we are studying is the contribution of gut microbes to the degradation of dietary toxins in insects, namely root fly larvae. These insect larvae reduce the yield of crucifer crops (rapeseed, cabbages) by up to 50% and are thus a serious risk to our biofuel and food industry. The key to their success is the detoxification of plant-derived secondary metabolites that repel generalist insects. Elucidating microbial breakdown
pathways by analysing the insect gut metagenome combined with investigating the respective enzyme pathways biochemically paves the way for a thorough understanding of this mode of microbe–insect relationship. With over one million insects species on our planet, we need to learn more about the contribution of microbes to the wellbeing and lifestyle of insects (Thompson and Brune, 2013), far beyond the few insect model systems that are investigated today. Looking into the crystal ball, we predict that knowledgeable biochemists and bio-informaticians will need to work hand in hand to understand each other’s trades and integrate it into a novel metagenome-driven but biochemically and physiologically validated microbial ecology. As the microbial world proves to be increasingly complex and diverse, the use of 16S rRNA genes and other phylogenetic marker will still be important for cataloguing our environment but will become less important in predicting physiological functions. They will instead be replaced by the analysis of full genome sequences that are more easily available with current and future techniques and that comprise more valuable and reliable information. Only if we know all microbial species on our planet, the phylomarker– microbial function relationship will become valid, and we are still a far way off. The knowledge from metagenomes needs to be taken one step further, to enrich and co-cultivate microbes and test the hypotheses deducted from the genome information. Ten years ago, we could only look at biogeochemical profiles – which are still astonishingly useful! – but today we can get a glimpse into nearly full genome sequences to adjust and improve our enrichment conditions. We need to train the new generation of microbiologists accordingly, not limiting ourselves to one specialization in both research and teaching of students. Establishing new master of science programmes and graduate schools targeting (meta)genomics, biochemistry and microbial physiology skills will be instrumental in this quest to broaden the microbial ecology horizon. Thus we are very fortunate that the Netherlands Government and Radboud University has affirmed the importance of microbiology by granting a so-called gravitation programme to establish the Soehngen Institute of Anaerobic Microbiology and a research master microbiology. In this way, we will be able to facilitate the education of this new generation of microbiologists. Special attention will also be paid to gender equality and leadership training to be able to continue the strong and leading school of Dutch Microbiology that will undoubtedly unravel many more exciting secrets of our fascinating newly discovered anaerobic microorganism. Gelukkig zij die nu beginnen! Fortunate those that are starting now! (Beijerinck) www.ru.nl/masters/microbiology www.ru.nl/microbiology
© 2015 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology Reports, 7, 23–25
Crystal ball
References Ettwig, K.F., Shima, S., van de Pas-Schoonen, K.T., Kahnt, J., Medema, M.H., Op den Camp, H.J., et al. (2008) Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ Microbiol 10: 3164–3173. Haroon, M.F., Hu, S., Shi, Y., Imelfort, M., Keller, J., Hugenholtz, P., et al. (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500: 567–570. Kartal, B., Geerts, W., and Jetten, M.S. (2011) Cultivation, detection, and ecophysiology of anaerobic ammoniumoxidizing bacteria. Methods Enzymol 486: 89–108. Kartal, B., de Almeida, N.M., Maalcke, W.J., Op den Camp, H.J., Jetten, M.S., and Keltjens, J.T. (2013) How to make a living from anaerobic ammonium oxidation. FEMS Microbiol Rev 37: 428–461. Kip, N., van Winden, J.F., Pan, Y., Bodrossy, L., Reichart, G.J., Smolders, A.J.P., et al. (2010) Global prevalence of methane oxidation by symbiotic bacteria in peat-moss ecosystems. Nat Geosci 3: 617–621. Larmola, T., Leppanen, S.M., Tuittila, E.S., Aarva, M., Merila, P., Fritze, H., and Tiirola, M. (2014) Methanotrophy induces nitrogen fixation during peatland development. Proc Natl Acad Sci USA 111: 734–739. Maalcke, W.J., Dietl, A., Marritt, S.J., Butt, J.N., Jetten, M.S., Keltjens, J.T., et al. (2014) Structural basis of biological NO generation by octaheme oxidoreductases. J Biol Chem 289: 1228–1242.
25
van Niftrik, L., and Jetten, M.S. (2012) Anaerobic ammoniumoxidizing bacteria: unique microorganisms with exceptional properties. Microbiol Mol Biol Rev 76: 585–596. Raghoebarsing, A.A., Smolders, A.J., Schmid, M.C., Rijpstra, W.I., Wolters-Arts, M., Derksen, J., et al. (2005) Methanotrophic symbionts provide carbon for photosynthesis in peat bogs. Nature 436: 1153–1156. Raghoebarsing, A.A., Pol, A., van de Pas-Schoonen, K.T., Smolders, A.J., Ettwig, K.F., Rijpstra, W.I., et al. (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440: 918–921. Russ, L., Speth, D.R., Jetten, M.S., Op den Camp, H.J., and Kartal, B. (2014) Interactions between anaerobic ammonium and sulfur-oxidizing bacteria in a laboratory scale model system. Environ Microbiol [Epub ahead of print]. doi:10.1111/1462-2920.12487. Sharon, I., and Banfield, J.F. (2013) Microbiology. Genomes from metagenomics. Science 342: 1057–1058. Strous, M., Heijnen, J.J., Kuenen, J.G., and Jetten, M.S.M. (1998) The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol 50: 589–596. Strous, M., Pelletier, E., Mangenot, S., Rattei, T., Lehner, A., Taylor, M.W., et al. (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440: 790–794. Thompson, C.L., and Brune, A. (2013) Crystal ball. Environ Microbiol Rep 5: 1–16. Wrighton, K.C., Castelle, C.J., Wilkins, M.J., Hug, L.A., Sharon, I., Thomas, B.C., et al. (2014) Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer. ISME J 8: 1452–1463. Yan, J., Haaijer, S.C., Op den Camp, H.J., van Niftrik, L., Stahl, D.A., Konneke, M., et al. (2012) Mimicking the oxygen minimum zones: stimulating interaction of aerobic archaeal and anaerobic bacterial ammonia oxidizers in a laboratory-scale model system. Environ Microbiol 14: 3146–3158.
© 2015 Society for Applied Microbiology and John Wiley & Sons Ltd, Environmental Microbiology Reports, 7, 23–25
