Education

 
1975     MSc in Biology at the State University of Groningen (the Netherlands); subjects General, Medical and Biochemical Microbiology

1978     PhD in Science at the State University of Groningen: Physiology and ecology of amino acid-fermenting bacteria isolated from anoxic wastewater treatment plants (promotor Prof. Hans Veldkamp)

  

Professional appointments

 
2009 to date Senior Scientist NIOO - KNAW 
2008 to date Research Associate Smithsonian Institute, Washington
2004 – 2016  Professor in Microbial Ecology of Wetlands, Utrecht University 
2001 – 2009 Director NIOO – Centre for Limnology, Nieuwersluis
1993 – 2001 Director of Science NIOO – Centre for Limnology, Nieuwersluis
1990 – 2005 Private chair in Soil Biology, Radboud University, Nijmegen
1985 – 1993 Head Department of Soil Biology, Institute of Ecological Research, Heteren
1983 – 1985 Scientist, Delta Institute for Hydrobiological Research, Yerseke
1980 – 1983 Post doc, State University of Groningen
1979 – 1980 Post doc, Georg August Universität, Göttingen, Germany 
 

Services to the profession (selection)

 
Editor FEMS Microbiology Ecology
 

Expertise

 
• Niche differentiation within microbial groups performing key geochemical processes
The microbial world can be subdivided in groups responsible for performing specific functions in the ecosystem, among which biogeochemical processes. Members of a functional group are likely to differ among each other in the rate at which they perform a particular process and in their responses to environmental conditions, thereby providing a potential link between group composition, niche differentiation and rates of biogeochemical processes. Microorganisms with overlapping functional traits are the appropriate model organisms to assess the significance of diversity for geochemical fluxes and to test general ecological principles such as adaptation through phenotypic plasticity and genotypic changes. Ammonia-oxidizing and sulfate-reducing microorganisms have been chosen to study niche differentiation within microbial groups performing key geochemical processes. Ammonia-oxidizing microorganisms are at the beginning of many environmental problems such as eutrophication, groundwater pollution, greenhouse gas emissions and soil acidification. By the production of sulfide, sulfate-reducing micro-organisms are involved in the immobilization of metals and in the internal phosphate eutrophication  
 
• Ammonia-oxidizing microorganisms
Aerobic ammonia-oxidizing microorganisms belong to the proteobacteria or the thaumarchaea. They share the ability to oxidize ammonia to nitrite and hence link the reduced and oxidized parts of the global nitrogen cycle. In contrast to the already long-known proteobacteria, relatively less is known about the recently discovered ammonia-oxidizing thaumarchaea, although their amoA genes outnumber those of the proteobacteria in many habitats suggesting an important role in the global nitrogen cycle. The diversity of the proteobacteria is restricted to only small number of species. However, the species behave in different ways with respect to environmental conditions, which indicate niche differentiation between the species. In the Scheldt estuary, for example, the dominant freshwater species is replaced by a salt-tolerant species. Surprisingly, the salt-tolerant species grows better under freshwater conditions compared to brackish circumstances, but are apparently overgrown by the others in the freshwater part of the estuary. It is not know if replacement of species has consequences for the rate of ammonia oxidation in the ecosystem. This question is tackled by studying the distribution of species in different environments by application of genetic methods aiming at specific phylogenetic or functional genes and by linking the patterns of distribution to patterns of physical and chemical characteristics. In addition, the behavior of isolated species is studied in model systems under controlled conditions in the laboratory. In this way, chemolithotrophic ammonia-oxidizing microorganisms are good model organisms for studying a possible relation between species identity and ecosystem functioning.
 
• Sulfate-reducing microorganisms
With respect to habitat, physiology and diversity, sulfate-reducing microorganisms are just the opposite of ammonia-oxidizing microorganisms. They thrive in anoxic environments, they require organic compounds for the generation of energy and they are much more diverse. However, despite the differences, the ecology of sulfate-reducing and ammonia-oxidizing microorganisms is studied in a similar way by looking to their distribution in different environments with the application of genetic tools based on a functional gene, and by investigating these microbes in model systems under controlled conditions in the laboratory.
 
 

PhD students supervised

 
Frank Verhagen (PhD thesis 1992), Willem Engelaar (1994), Paul Bodelier (1997), Ronald Kester (1997), Joke Nijburg (1998), Erik van Hannen (1999), Jaco van der Nat (2000), Arjen Speksnijder (2000), Monique de Bie (2002), Jody de Brouwer (2002), Nicole Wrage (2003), Marco Dignum (2003), Marc Staal (2003), Jolanda Verspagen (2006), Stefan Simis (2006), Martijn Antheunisse (2007), Marjolijn Tijdens (2007), Manuela Coci (2007), Marzia Miletto (2007), Juanjuan Wang (2011), Liesbeth Vissers (2012), Susann Vollrath (2012), Anne Steenbergh (2012), Joost Keuskamp (2014) and Anne Daebeler (2014).
 

 

Centre for Wetland Ecology
The Centre for Wetland Ecology (http://www.wetland-ecology.nl/) is a formal collaboration between the NIOO and the universities of Nijmegen, Amsterdam and Utrecht in which ecologists, ecophysiologists and biogeochemists work together for a better understanding of the functioning of wetlands. The research ranges from the functioning of individual animals, bacteria and plants in their natural wetland environment to the behaviour of ecosystems and landscapes.

Nitrification Network
The objectives of the Nitrification Network are to coordinate research activities of the participants where multi-investigator proposals and projects are called for and to coordinate meetings of interest to members of the Nitrification Network and others in the field.

 

 

Most recent publications

Laanbroek HJ, Veenhuizen PTM, Keijzer RA, Hefting MM (2017) Numerical relationships between archaeal and bacterial amoA genes vary by Icelandic Andosol classes. Microbial Ecology (online)

ABSTRACT: Bacterial amoA genes had not been detectable by qPCR in freshly sampled Icelandic Andosols thus far. Hence, a new primer set yielding shorter gene fragments has been designed to verify the absence of ammonia-oxidizing bacteria in different Icelandic Andosol classes. At the same time, a new primer set was also constructed for archaeal amoA genes that should improve the quality of PCR products. Although a large part of the soil samples were found to be amoA-negative, bacterial amoA genes were detectable with new as well as old primer sets. The same results were obtained for the archaeal amoA genes. The relative distribution of archaeal and bacterial amoA genes varied between Andosol classes. Archaeal amoA genes were significantly more abundant in Brown than in Histic Andosols, while the opposite was observed for bacterial amoA genes. The numbers of archaeal and bacterial amoA genes in Gleyic Andosols were not significantly different from those in Histic and Brown Andosols. The numbers of bacterial amoA genes, but not the numbers of archaeal amoA genes, correlated significantly and positively with potential ammonia oxidation activities. The presence of the bacterial nitrification inhibitor allylthiourea inhibited the potential ammonia oxidation activities during the first 12 h of incubation.

 

Daebeler A, Bodelier PLE, Hefting MM, Rütting T, Laanbroek (2017) Soil warming and fertilization altered rates of nitrogen transformation processes and selected for adapted ammonia-oxidizing archaea in sub-arctic grassland soil. Soil Biology and Biochemistry 107: 114-124

ABSTRACT: The balance of microbial nitrogen (N) transformation processes in sub-arctic terrestrial ecosystems is most likely affected by global change, with potential feedbacks to greenhouse gas emissions and eutrophication. Soil temperature and N availability e their global increases being two of the most pressing global change features - will be prime drivers of N dynamics and microbial community structure, but little is known about their interactive effects in these ecosystems. We utilized geothermally warmed soils from Iceland as a natural experiment for assessing fertilization and warming effects on gross soil N transformation processes. Experimental incubations of these soils at different temperatures coupled with a dual 15N-labelling/-tracing approach and pyrotag transcript-sequencing allowed for the analysis of independent and combined impacts of N fertilization and temperature shifts on gross N mineralization, nitrification, and ammonium and nitrate immobilization rates and archaeal ammonia-oxidizing (AOA) communities, being the key ammonia oxidizers in this soil. Gross nitrification in warmed soil was increased in relation to ambient temperature soil and exhibited a higher temperature optimum. Concomitantly, our results revealed a selection of AOA populations adapted to in situ soil temperatures. Phylogenetically distinct populations of actively ammonia-oxidizing archaea exhibited conserved temperature optima. N mineralization and nitrification showed higher sensitivities in response to short-term temperature changes if the soils had been warmed. In part, the influence of short-term temperature changes could however be neutralized by the effects of N fertilization. Long-term N fertilization alone affected only gross N mineralization. However, all gross N transformation rates were significantly altered by the interactive effects of N fertilization and soil warming. We conclude that in order to reliably predict effects of global change on sub-arctic soil N transformation processes we need to consider multiple interactions among global change factors and to take into account the capacity of soil microbial populations to adapt to global change conditions.

 

Balk M, Keuskamp JA, Laanbroek HJ (2016) Potential for sulfate reduction in mangrove forest soils: Comparison between two dominant species of the Americas. Frontiers of Microbiology 7, Article 1855

ABSTRACT: Avicennia and Rhizophora are globally occurring mangrove genera with different traits that place them in different parts of the intertidal zone. It is generally accepted that the oxidizing capacity of Avicennia roots is larger than that of Rhizophora roots, which initiates more reduced conditions in the soil below the latter genus. We hypothesize that the more reduced conditions beneath Rhizophora stands lead to more active sulfate-reducing microbial communities compared to Avicennia stands. To test this hypothesis, we measured sulfate reduction traits in soil samples collected from neighboring Avicennia germinans and Rhizophora mangle stands at three different locations in southern Florida. The traits measured were sulfate reduction rates (SRR) in flow-through reactors containing undisturbed soil layers in the absence and presence of easily degradable carbon compounds, copy numbers of the dsrB gene, which is specific for sulfate-reducing microorganisms, and numbers of sulfate-reducing cells that are able to grow in liquid medium on a mixture of acetate, propionate and lactate as electron donors. At the tidal locations Port of the Islands and South Hutchinson Islands, steady state SRR, dsrB gene copy numbers and numbers of culturable cells were higher at the A. germinans than at the R. mangle stands, although not significantly for the numbers at Port of the Islands. At the non-tidal location North Hutchinson Island, results are mixed with respect to these sulfate reduction traits. At all locations, the fraction of culturable cells were significantly higher at the R. mangle than at the A. germinans stands. The dynamics of the initial SRR implied a more in situ active sulfate-reducing community at the intertidal R. mangle stands. It was concluded that in agreement with our hypothesis R. mangle stands accommodate a more active sulfate-reducing community than A. germinans stands, but only at the tidal locations. The differences between R. mangle and A. germinans stands were absent at the non-tidal, impounded location.

 

Rice MC, Norton JM, Valois F, Bollmann A, Bottomley PJ, Klotz MG, Laanbroek HJ, Suwa Y, Stein LY, Sayavedra-Soto L, Woyke T, Shapiro N, Goodwin LA, Huntemann M, Clum A, Pillay M, Kyrpides N, Varghese N, Mikhailova N, Markowitz V, Palaniappan K, Ivanova N, Stamatis D, Reddy TBK, Ngan CY, Daum C (2016) Complete genome of Nitrosospira briensis C-128, an ammonia-oxidizing bacterium from agricultural soil. Standards in Genomic Sciences 11 (2016) 46

ABSTRACT: Nitrosospira briensis C-128 is an ammonia-oxidizing bacterium isolated from an acid agricultural soil. N. briensis C-128 was sequenced with PacBio RS technologies at the DOE-Joint Genome Institute through their Community Science Program (2010). The high-quality finished genome contains one chromosome of 3.21 Mb and no plasmids. We identified 3073 gene models, 3018 of which are protein coding. The two-way average nucleotide identity between the chromosomes of Nitrosospira multiformis ATCC 25196 and Nitrosospira briensis C-128 was found to be 77.2 %. Multiple copies of modules encoding chemolithotrophic metabolism were identified in their genomic context. The gene inventory supports chemolithotrophic metabolism with implications for function in soil environments.

 

Soares J, Cassman N, Kielak A, Pijl A, Carmo J,  Lourenço K, Laanbroek H, Cantarella H, Kuramae E (201x) Nitrous oxide emission related to ammonia-oxidizing bacteria and mitigation options during sugarcane growth in a tropical soil. Scientific Reports 6 (2016) srep 30349

ABSTRACT: Nitrous oxide (N2O) from nitrogen fertilizers applied to sugarcane has high environmental impact on ethanol production. This study aimed to determine the main microbial processes responsible for the N2O emissions from soil fertilized with different N sources, to identify options to mitigate N2O emissions, and to determine the impacts of the N sources on the soil microbiome. In a field experiment, nitrogen was applied as calcium nitrate, urea, urea with dicyandiamide or 3,4 dimethylpyrazone phosphate nitrification inhibitors (NIs), and urea coated with polymer and sulfur (PSCU). Urea caused the highest N2O emissions (1.7% of N applied) and PSCU did not reduce cumulative N2O emissions compared to urea. NIs reduced N2O emissions (95%) compared to urea and had emissions comparable to those of the control (no N). Similarly, calcium nitrate resulted in very low N2O emissions. Interestingly, N2O emissions were significantly correlated only with bacterial amoA, but not with denitrification gene (nirK, nirS, nosZ) abundances, suggesting that ammonia-oxidizing bacteria, via the nitrification pathway, were the main contributors to N2O emissions. Moreover, the treatments had little effect on microbial composition or diversity. We suggest nitrate-based fertilizers or the addition of NIs in NH4 +-N based fertilizers as viable options for reducing N2O emissions in tropical soils and lessening the environmental impact of biofuel produced from sugarcane.

 

Sedlacek CJ, Nielsen S, Greis KD, Haffey WD,  Revsbech NP, Ticak T, Laanbroek HJ, Bollmann A (2016) Effects of Bacterial Community Members on the Proteome of the Ammonia-Oxidizing Bacterium Nitrosomonas sp. Strain Is79. Applied and Environmental Microbiology 82: 4776-4788

Microorganisms in the environment do not exist as the often-studied pure cultures but as members of complex microbial communities. Characterizing the interactions within microbial communities is essential to understand their function in both natural and engineered environments. In this study, we investigated how the presence of a nitrite-oxidizing bacterium (NOB) and heterotrophic bacteria affect the growth and proteome of the chemolithoautotrophic ammonia-oxidizing bacterium (AOB) Nitrosomonas sp. strain Is79. We investigated Nitrosomonas sp. Is79 in co-culture with Nitrobacter winogradskyi, in co-cultures with selected heterotrophic bacteria, and as a member of the nitrifying enrichment culture G5-7. In batch culture, N. winogradskyi and heterotrophic bacteria had positive effects on the growth of Nitrosomonas sp. Is79. An isobaric tag for relative and absolute quantification (iTRAQ) liquid chromatography-tandem mass spectrometry (LC-MS/MS) proteomics approach was used to investigate the effect of N. winogradskyi and the co-cultured heterotrophic bacteria from G5-7 on the proteome of Nitrosomonas sp. Is79. In co-culture with N. winogradskyi, several Nitrosomonas sp. Is79 oxidative stress response proteins changed in abundance, with periplasmic proteins increasing and cytoplasmic proteins decreasing in abundance. In the presence of heterotrophic bacteria, the abundance of proteins directly related to the ammonia oxidation pathway increased, while the abundance of proteins related to amino acid synthesis and metabolism decreased. In summary, the proteome of Nitrosomonas sp. Is79 was differentially influenced by the presence of either N. winogradskyi or heterotrophic bacteria. Together, N. winogradskyi and heterotrophic bacteria reduced the oxidative stress for Nitrosomonas sp. Is79, which resulted in more efficient metabolism.

IMPORTANCE

Aerobic ammonia-oxidizing microorganisms play an important role in the global nitrogen cycle, converting ammonia to nitrite. In their natural environment, they coexist and interact with nitrite oxidizers, which convert nitrite to nitrate, and with heterotrophic microorganisms. The presence of nitrite oxidizers and heterotrophic bacteria has a positive influence on the growth of the ammonia oxidizers. Here, we present a study investigating the effect of nitrite oxidizers and heterotrophic bacteria on the proteome of a selected ammonia oxidizer in a defined culture to elucidate how these two groups improve the performance of the ammonia oxidizer. The results show that the presence of a nitrite oxidizer and heterotrophic bacteria reduced the stress for the ammonia oxidizer and resulted in more efficient energy generation. This study contributes to our understanding of micro-microbe interactions, in particular between ammonia oxidizers and their neighboring microbial community.

 

Top-ten most cited publications (Web of Science July 2017)

1.  Bodelier PLE, Laanbroek HJ (2004) Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiology Ecology 47: 265-277 (314 citations)

2.  Van Hannen EJ, Zwart GJM, van Agterveld MP, Gons HJ, Ebert J, Laanbroek HJ (1999) Changes in the bacterial and eukaryotic community structure after mass lysis of filamentous cyanobacteria associated with viruses. Applied and Environmental Microbiology 65: 795-801 (190 citations)

3.  Speksnijder AGCL, Kowalchuk GA, de Jong S, Kline E, Stephen JR, Laanbroek HJ (2001) Micro-variation artefacts introduced by PCR and cloning of closely related 16S rDNA sequences. Applied and Environmental Microbiology 67: 469-472 (175 citations)

4.  Laanbroek HJ, Pfennig N (1981) Oxidation of short-chain fatty acids by sulphate-reducing bacteria in freshwater and in marine sediments. Archive of Microbiology 128: 330-335 (173 citations)

5.  Van Hannen EJ, Mooij WM, Van Agterveld MP, Gons HJ, Laanbroek HJ (1999) Detritus-dependent development of the microbial community in an experimental system: A quantitative analysis using denaturing gradient gel electrophoresis. Applied (and) Environmental Microbiology 65: 2478-2484 (151 citations)

6.  Kowalchuk GA, Bodelier PLE, Heilig GHJ, Stephen JR, Laanbroek HJ (1998) Community analysis of ammonia-oxidising bacteria in relation to oxygen-availability in soils and root-oxygenated sediments, using PCR, DGGE and oligonucleotide probe hybridisation. FEMS Microbiology Ecology 27: 339-350 (149 citations)

7.  Bodelier PLE, Libochant JA, Blom CWPM, Laanbroek HJ (1996) Dynamics of nitrification and denitrification in root-oxygenated sediments and adaptation of ammonia-oxidizing bacteria to low oxygen or anoxic habitats. Applied and Environmental Microbiology 62: 4100-4107 (144 citations)

8. Verhagen FJM, Laanbroek HJ (1991) Competition for ammonium between nitrifying and heterotrophic bacteria in energy limited chemostats. Applied and Environmental Microbiology 57: 3255-3263 (140 citations)

9.  Zwart G, Hiorns WD, Methé BA, van Agterveld MP, Huismans R, Nold SC, Zehr JP, Laanbroek HJ (1998) Nearly identical 16S rRNA sequences recovered from lakes in North America and Europe indicate the existence of clades of freshwater bacteria with global distribution. Systematic and Applied Microbiology 21:546-556 (138 citations)

10.  Laanbroek HJ, Gerards S (1993) Competition for limiting amounts of oxygen between Nitrosomonas europaea and Nitrobacter winogradskyi grown in mixed continuous cultures. Archive of Microbiology 159: 453-459 (129 citations)

Ecology & Biodiversity Group

Institute of Environmental Biology

Utrecht University

http://www.uu.nl/en/research/ecology-and-biodiversity

 

Centre for Wetland Ecology

http://www.wetland-ecology.nl/

 

Nitrification Network

http://nitrificationnetwork.org/

 

ResearcherID: http://www.researcherid.com/Workspace.action

ORCID: http://orcid.org/0000-0003-2400-3399