Papers by Matthias Labrenz
Environmental Microbiology, 2013
Barrier zones between oxic and anoxic water masses (redoxclines) host highly active prokaryotic c... more Barrier zones between oxic and anoxic water masses (redoxclines) host highly active prokaryotic communities with important roles in biogeochemical cycling. In Baltic Sea pelagic redoxclines, Epsilonproteobacteria of the genus Sulfurimonas (subgroup GD17) have been shown to dominate chemoautotrophic denitrification. However, little is known on the loss processes affecting this prokaryotic group. In the present study, the protist grazing impact on the Sulfurimonas subgroup GD17 was determined for suboxic and oxygen/hydrogen sulphide interface depths of Baltic Sea redoxclines, using predator exclusion assays and bacterial amendment with the cultured representative 'Sulfurimonas gotlandica' strain GD1. Additionally, the principal bacterivores were identified by RNA-Stable Isotope Probing (RNA-SIP). The natural Sulfurimonas subgroup GD17 population grew strongly under oxygen/hydrogen sulphide interface conditions (doubling time: 1-1.5 days), but protist grazing could consume the complete new cell production per day. In suboxic samples, little or no growth of Sulfurimonas subgroup GD17 was observed. RNA-SIP identified five active grazers, belonging to typical redoxcline ciliates (Oligohymenophorea, Prostomatea) and globally widespread marine flagellate groups (MAST-4, Chrysophyta, Cercozoa). Overall, we demonstrate for the first time that protist grazing can control the growth, and potentially the vertical distribution, of a chemolithoautotrophic key-player of oxic/anoxic interfaces.
Steep redoxclines form between oxic surface water and the stagnant, sulfidic hypolimnion in the e... more Steep redoxclines form between oxic surface water and the stagnant, sulfidic hypolimnion in the eutrophied, brackish water Baltic Sea. Nitrification, denitrification, and anammox were measured at and below the redoxcline to quantify the role of water-column nitrogen processes in the overall magnitude of nitrogen removal in the Baltic Sea. Rates of nitrification were very high (up to 85 nmol N L 21 d 21 ) at the oxic-anoxic interface, but, surprisingly, nitrification was separated from the processes reducing nitrate to N 2 (up to 810 nmol N L 21 d 21 ) by tens of meters in depth. N 2 production was dominated by chemolithotrophic denitrification, with anammox playing only a negligible role, and limited to the water layers in which nitrite or nitrate coexisted with sulfide. The alternating oxygen concentrations in the basin induce irregular bursts of nitrogen removal. Nitrification takes place after mixing of ammonium-rich deep water with oxic water, and denitrification uses the formed nitrite and nitrate once anoxic conditions re-establish. Although removal rates can be high, conditions allowing such rates are likely short-lived. While the sedimentary denitrification rates at the shallower, oxic areas are lower, they are more constant in time, highlighting the need to avoid hypoxia, which would prevent sedimentary denitrification.
Applied and environmental microbiology, 2004
We have developed a highly sensitive approach to assess the abundance of uncultured bacteria in w... more We have developed a highly sensitive approach to assess the abundance of uncultured bacteria in water samples from the central Baltic Sea by using a noncultured member of the "Epsilonproteobacteria" related to Thiomicrospira denitrificans as an example. Environmental seawater samples and samples enriched for the target taxon provided a unique opportunity to test the approach over a broad range of abundances. The approach is based on a combination of taxon- and domain-specific real-time PCR measurements determining the relative T. denitrificans-like 16S rRNA gene and 16S rRNA abundances, as well as the determination of total cell counts and environmental RNA content. It allowed quantification of T. denitrificans-like 16S rRNA molecules or 16S rRNA genes as well as calculation of the number of ribosomes per T. denitrificans-like cell. Every real-time measurement and its specific primer system were calibrated using environmental nucleic acids obtained from the original habita...
Environmental Science & Technology, 2014
Chemolithoautotrophic denitrification is an important mechanism of nitrogen loss in the water col... more Chemolithoautotrophic denitrification is an important mechanism of nitrogen loss in the water column of euxinic basins, but its isotope fractionation factor is not known. Sulf urimonas gotlandica GD1 T , a recently isolated bacterial key player in Baltic Sea pelagic redoxcline processes, was used to determine the isotope fractionation of nitrogen and oxygen in nitrate during denitrification. Under anoxic conditions, nitrate reduction was accompanied by nitrogen and oxygen isotope fractionation of 23.8 ± 2.5‰ and 11.7 ± 1.1‰, respectively. The isotope effect for nitrogen was in the range determined for heterotrophic denitrification, with only the absence of stirring resulting in a significant decrease of the fractionation factor. The relative increase in δ 18 O NO3 to δ 15 N NO3 did not follow the 1:1 relationship characteristic of heterotrophic, marine denitrification. Instead, δ 18 O NO3 increased slower than δ 15 N NO3, with a conserved ratio of 0.5:1. This result suggests that the periplasmic nitrate reductase (Nap) of S. gotlandica strain GD1 T fractionates the N and O in nitrate differently than the membrane-bound nitrate reductase (Nar), which is generally prevalent among heterotrophic denitrifiers and is considered as the dominant driver for the observed isotope fractionation. Hence in the Baltic Sea redoxcline, other, as yet-unidentified factors likely explain the low apparent fractionation.
Systematic and Applied Microbiology, 2014
The ISME Journal, 2011
Salinity is a major factor controlling the distribution of biota in aquatic systems, and most aqu... more Salinity is a major factor controlling the distribution of biota in aquatic systems, and most aquatic multicellular organisms are either adapted to life in saltwater or freshwater conditions. Consequently, the saltwater-freshwater mixing zones in coastal or estuarine areas are characterized by limited faunal and floral diversity. Although changes in diversity and decline in species richness in brackish waters is well documented in aquatic ecology, it is unknown to what extent this applies to bacterial communities. Here, we report a first detailed bacterial inventory from vertical profiles of 60 sampling stations distributed along the salinity gradient of the Baltic Sea, one of world's largest brackish water environments, generated using 454 pyrosequencing of partial (400 bp) 16S rRNA genes. Within the salinity gradient, bacterial community composition altered at broad and finer-scale phylogenetic levels. Analogous to faunal communities within brackish conditions, we identified a bacterial brackish water community comprising a diverse combination of freshwater and marine groups, along with populations unique to this environment. As water residence times in the Baltic Sea exceed 3 years, the observed bacterial community cannot be the result of mixing of fresh water and saltwater, but our study represents the first detailed description of an autochthonous brackish microbiome. In contrast to the decline in the diversity of multicellular organisms, reduced bacterial diversity at brackish conditions could not be established. It is possible that the rapid adaptation rate of bacteria has enabled a variety of lineages to fill what for higher organisms remains a challenging and relatively unoccupied ecological niche.
The ISME Journal, 2013
The Baltic Sea receives large nitrogen inputs by diazotrophic (N 2 -fixing) heterocystous cyanoba... more The Baltic Sea receives large nitrogen inputs by diazotrophic (N 2 -fixing) heterocystous cyanobacteria but the significance of heterotrophic N 2 fixation has not been studied. Here, the diversity, abundance and transcription of the nifH fragment of the nitrogenase enzyme in two basins of the Baltic Sea proper was examined. N 2 fixation was measured at the surface (5 m) and in anoxic water (200 m). Vertical sampling profiles of 410 and o10 lm size fractions were collected in 2007, 2008 and 2011 at the Gotland Deep and in 2011 in the Bornholm Basin. Both of these stations are characterized by permanently anoxic bottom water. The 454-pyrosequencing nifH analysis revealed a diverse assemblage of nifH genes related to alpha-, beta-and gammaproteobacteria (nifH cluster I) and anaerobic bacteria (nifH cluster III) at and below the chemocline. Abundances of genes and transcripts of seven diazotrophic phylotypes were investigated using quantitative polymerase chain reaction revealing abundances of heterotrophic nifH phylotypes of up to 2.1 Â 10 7 nifH copies l À 1 . Abundant nifH transcripts (up to 3.2 Â 10 4 transcripts l À 1 ) within nifH cluster III and co-occurring N 2 fixation (0.44 ± 0.26 nmol l À 1 day À 1 ) in deep water suggests that heterotrophic diazotrophs are fixing N 2 in anoxic ammonium-rich waters. Our results reveal that N 2 fixation in the Baltic Sea is not limited to illuminated N-deplete surface waters and suggest that N 2 fixation could also be of importance in other suboxic regions of the world's oceans.
The ISME Journal, 2010
Proteorhodopsins (PRs) are light-driven proton pumps that have been found in a variety of marine ... more Proteorhodopsins (PRs) are light-driven proton pumps that have been found in a variety of marine environments. The goal of this study was to search for PR presence in different freshwater and brackish environments and to explore the diversity of non-marine PR protein. Here, we show that PRs exist in distinctly different aquatic environments, ranging from clear water lakes to peat lakes and in the Baltic Sea. Some of the PRs observed in this study formed unique clades that were not previously observed in marine environments, whereas others were similar to PRs found in non-marine samples of the Global Ocean Sampling (GOS) expedition. Furthermore, the similarity of several PRs isolated from lakes in different parts of the world suggests that these genes are dispersed globally and that they may encode unique functional capabilities enabling successful competition in a wide range of freshwater environments. Phylogenomic analysis of genes found on these GOS scaffolds suggests that some of the freshwater PRs are found in freshwater Flavobacteria and freshwater SAR11-like bacteria.
PLoS ONE, 2014
The biodegradability of terrigenous dissolved organic matter (tDOM) exported to the sea has a maj... more The biodegradability of terrigenous dissolved organic matter (tDOM) exported to the sea has a major impact on the global carbon cycle, but our understanding of tDOM bioavailability is fragmentary. In this study, the effects of preparative tDOM isolation on microbial decomposition were investigated in incubation experiments consisting of mesocosms containing mesohaline water from the Baltic Sea. Dissolved organic carbon (DOC) consumption, molecular DOM composition, bacterial activities, and shifts in bacterial community structure were compared between mesocosms supplemented with riverine tDOM, either as filtered, particle-free river water or as a concentrate obtained by lyophilization/tangential ultrafiltration, and those containing only Baltic Sea water or river water. As shown using ultra-high-resolution mass spectrometry (15 Tesla Fourier-transform ion cyclotron resonance mass spectrometry, FT-ICR-MS) covering approximately 4600 different DOM compounds, the three DOM preparation protocols resulted in distinct patterns of molecular DOM composition. However, despite DOC losses of 4-16% and considerable bacterial production, there was no significant change in DOM composition during the 28-day experiment. Moreover, tDOM addition affected neither DOC degradation nor bacterial dynamics significantly, regardless of the tDOM preparation. This result suggested that the introduced tDOM was largely not bioavailable, at least on the temporal scale of our experiment, and that the observed bacterial activity and DOC decomposition mainly reflected the degradation of unknown, labile, colloidal and low-molecular weight DOM, both of which escape the analytical window of FT-ICR-MS. In contrast to the different tDOM preparations, the initial bacterial inoculum and batch culture conditions determined bacterial community succession and superseded the effects of tDOM addition. The uncoupling of tDOM and bacterial dynamics suggests that mesohaline bacterial communities cannot efficiently utilize tDOM and that in subarctic estuaries other factors are responsible for the removal of imported tDOM.
INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, 2013
INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, 2002
An aerobic and heterotrophic isolate, designated IFAM EL-30 T , was obtained from hypersaline Ekh... more An aerobic and heterotrophic isolate, designated IFAM EL-30 T , was obtained from hypersaline Ekho Lake (Vestfold Hills, East Antarctica). The isolate consisted of Gram-positive cocci or short rods which occasionally exhibited branching. The organism was moderately halotolerant, required thiamin.HCl and was stimulated by biotin and nicotinic acid. It grew well with glucose, acetate, pyruvate, succinate, malate or glutamate, and hydrolysed DNA but not gelatin, starch or Tween 80. Nitrate was aerobically reduced to nitrite. Chemical analysis revealed diphosphatidylglycerol, phosphatidylglycerol, phosphatidylcholine and an unidentified glycolipid as the major polar lipids. The cellular fatty acids were predominantly of the anteiso and iso methylbranched types, and the major menaquinones were MK-7 and MK-8. The peptidoglycan type was A4α, L-Lys-L-Glu. The DNA base ratio was 661 mol % GMC. Comparisons of 16S rRNA gene sequences showed that the unidentified organism was phylogenetically closely related to Nesterenkonia halobia, although a sequence divergence value of S 3 % demonstrated that the organism represents a different species. On the basis of phenotypic and genotypic evidence, it is proposed that the unknown bacterium be designated as a new species of the genus Nesterenkonia, namely Nesterenkonia lacusekhoensis sp. nov., the type strain being IFAM EL-30 T (l DSM 12544 T l CIP 107030 T ). An emended description of the genus Nesterenkonia is given.
FEMS Microbiology Ecology, 2010
Oxic-anoxic interfaces harbor significant numbers and activity of chemolithoautotrophic microorga... more Oxic-anoxic interfaces harbor significant numbers and activity of chemolithoautotrophic microorganisms, known to oxidize reduced sulfur or nitrogen species. However, measurements of in situ distribution of bulk carbon dioxide (CO 2 ) assimilation rates and active autotrophic microorganisms have challenged the common concept that aerobic and denitrifying sulfur oxidizers are the predominant autotrophs in pelagic oxic-anoxic interfaces. Here, we provide a comparative investigation of nutrient, sulfur, and manganese chemistry, microbial biomass distribution, as well as CO 2 fixation at the pelagic redoxcline of the eastern Gotland Basin, Baltic Sea. Opposing gradients of oxygen, nitrate, and sulfide approached the detection limits at the chemocline at 204 m water depth. No overlap of oxygen or nitrate with sulfide was observed, whereas particulate manganese was detected down to 220 m. More than 70% of the bulk dark CO 2 assimilation, totaling 9.3 mmol C m À2 day À1 , was found in the absence of oxygen, nitrite, and nitrate and could not be stimulated by their addition. Maximum fixation rates of up to 1.1 mmol C L À1 day À1 were surprisingly susceptible to altered redox potential or sulfide concentration. These results suggest that novel redox-sensitive pathways of microbial sulfide oxidation could account for a significant fraction of chemolithoautotrophic growth beneath pelagic chemoclines. A mechanism of coupled activity of sulfur-oxidizing and sulfur-reducing microorganisms is proposed.
FEMS Microbiology Ecology, 2010
Marine pelagic redoxclines are characterized by pronounced activities of chemolithoautotrophic mi... more Marine pelagic redoxclines are characterized by pronounced activities of chemolithoautotrophic microorganisms. As evidenced by the high dark CO 2 fixation rates measured around the oxic-anoxic interface but also in the upper sulfidic zone, the accordant organisms participate in important biogeochemical transformations. Although Epsilonproteobacteria have been identified as an important chemoautotrophic group in these environments, detailed species-level information on the identity of actively involved prokaryotes is lacking. In the present study, active chemolithoautotrophic prokaryotic assemblages were identified in the sulfidic zone of a pelagic Black Sea redoxcline by applying rRNA-based stable isotope probing in combination with 16S rRNA gene single-strand conformation polymorphism analysis and 16S rRNA gene cloning. The results showed that a single epsilonproteobacterium, affiliated with the genus Sulfurimonas, and two different members of the gammaproteobacterial sulfur oxidizer (GSO) cluster were responsible for dark CO 2 fixation activities in the upper sulfidic layer of the Black Sea redoxcline. Phylogenetically, these organisms were closely related to microorganisms, distributed worldwide, that are thought to be key players in denitrification and sulfide oxidation. Together, these findings emphasize the importance of chemolithoautotrophic members of the Sulfurimonas and GSO groups in the carbon, nitrogen, and sulfur cycles of oxic-anoxic pelagic transition zones.
Barrier zones between oxic and anoxic water masses (redoxclines) host highly active prokaryotic c... more Barrier zones between oxic and anoxic water masses (redoxclines) host highly active prokaryotic communities with important roles in biogeochemical cycling. In Baltic Sea pelagic redoxclines, Epsilonproteobac-teria of the genus Sulfurimonas (subgroup GD17) have been shown to dominate chemoautotrophic denitrification. However, little is known on the loss processes affecting this prokaryotic group. In the present study, the protist grazing impact on the Sulfurimonas subgroup GD17 was determined for suboxic and oxygen/hydrogen sulphide interface depths of Baltic Sea redoxclines, using predator exclusion assays and bacterial amendment with the cultured representative 'Sulfurimonas gotlandica' strain GD1. Additionally, the principal bacterivores were identified by RNA-Stable Isotope Probing (RNA-SIP). The natural Sulfurimonas subgroup GD17 population grew strongly under oxygen/hydrogen sulphide interface conditions (doubling time: 1–1.5 days), but protist grazing could consume the complete new cell production per day. In suboxic samples, little or no growth of Sulfurimonas subgroup GD17 was observed. RNA-SIP identified five active grazers, belonging to typical redoxcline ciliates (Oligohy-menophorea, Prostomatea) and globally widespread marine flagellate groups (MAST-4, Chrysophyta, Cer-cozoa). Overall, we demonstrate for the first time that protist grazing can control the growth, and potentially the vertical distribution, of a chemolithoautotrophic key-player of oxic/anoxic interfaces.
Environmental Microbiology, 2014
Knowledge on Actinobacteria rhodopsin gene (actR) diversity and spatial distribution is scarce. T... more Knowledge on Actinobacteria rhodopsin gene (actR) diversity and spatial distribution is scarce. The Baltic Sea is characterized by strong salinity gradients leading to the coexistence of marine and freshwater bacteria and hence is an ideal study area to elucidate the dispersion and phylogenetic affiliation of actR in dependence on salinity. ActR DGGE fingerprints in summer 2008 revealed between 3 and 19 distinct bands within a salinity range of 2.4-27 PSU. Environmental actR clone sequences were obtained from stations distributed along the whole salinity gradient. Overall, 20 different actR sequence groups (operational taxonomic units) were found, with up to 11 different ones per station. Phylogenetically, the actR sequences were predominantly (80%) affiliated with freshwater acI-Actinobacteria whose 16S rRNA gene accounted for 2-33% of total 16S rRNA genes in both the Bothnian Sea and central Baltic Sea. However, at salinities above 14 PSU, acI-16S rRNA gene accounted for less than 1%. In contrast, the diversity of actR remained high. Changes in actR gene diversity were significantly correlated with salinity, oxygen, silica or abundance of Synechococcus sp. Our results demon-strate a wide distribution of freshwater actR along the Baltic Sea salinity gradient indicating that some freshwater Actinobacteria might have adapted to higher salinities.
Aquatic Microbial Ecology, 2008
We now have a relatively good idea of how bulk microbial processes shape the cycling of organic m... more We now have a relatively good idea of how bulk microbial processes shape the cycling of organic matter and nutrients in the sea. The advent of the molecular biology era in microbial ecology has resulted in advanced knowledge about the diversity of marine microorganisms, suggesting that we might have reached a high level of understanding of carbon fluxes in the oceans. However, it is becoming increasingly clear that there are large gaps in the understanding of the role of bacteria in regulating carbon fluxes. These gaps may result from methodological as well as conceptual limitations. For example, should bacterial production be measured in the light? Can bacterial production conversion factors be predicted, and how are they affected by loss of tracers through respiration? Is it true that respiration is relatively constant compared to production? How can accurate measures of bacterial growth efficiency be obtained? In this paper, we discuss whether such questions could (or should) be addressed. Ongoing genome analyses are rapidly widening our understanding of possible metabolic pathways and cellular adaptations used by marine bacteria in their quest for resources and struggle for survival (e.g. utilization of light, acquisition of nutrients, predator avoidance, etc.). Further, analyses of the identity of bacteria using molecular markers (e.g. subgroups of Bacteria and Archaea) combined with activity tracers might bring knowledge to a higher level. Since bacterial growth (and thereby consumption of DOC and inorganic nutrients) is likely regulated differently in different bacteria, it will be critical to learn about the life strategies of the key bacterial species to achieve a comprehensive understanding of bacterial regulation of C fluxes. Finally, some processes known to occur in the microbial food web are hardly ever characterized and are not represented in current food web models. We discuss these issues and offer specific comments and advice for future research agendas.
Applied and Environmental Microbiology, 2005
Anaerobic or microaerophilic chemolithoautotrophic bacteria have been considered to be responsibl... more Anaerobic or microaerophilic chemolithoautotrophic bacteria have been considered to be responsible for CO 2 dark fixation in different pelagic redoxclines worldwide, but their involvement in redox processes is still not fully resolved. We investigated the impact of 17 different electron donor/acceptor combinations in water of pelagic redoxclines from the central Baltic Sea on the stimulation of bacterial CO 2 dark fixation as well as on the development of chemolithoautotrophic populations. In situ, the highest CO 2 dark fixation rates, ranging from 0.7 to 1.4 mol liter ؊1 day ؊1 , were measured directly below the redoxcline. In enrichment experiments, chemolithoautotrophic CO 2 dark fixation was maximally stimulated by the addition of thiosulfate, reaching values of up to 9.7 mol liter ؊1 CO 2 day ؊1 . Chemolithoautotrophic nitrate reduction proved to be an important process, with rates of up to 33.5 mol liter ؊1 NO 3 ؊ day ؊1 .
Applied and Environmental Microbiology, 2006
Identification and functional analysis of key members of bacterial communities in marine and estu... more Identification and functional analysis of key members of bacterial communities in marine and estuarine environments are major challenges for obtaining a mechanistic understanding of biogeochemical processes. In the Baltic Sea basins, as in many other marine environments with anoxic bodies of water, the oxic-anoxic interface is considered a layer of high bacterial turnover of sulfur, nitrogen, and carbon compounds that has a great impact on matter balances in the whole ecosystem. We focused on autotrophic denitrification by oxidation of reduced sulfur compounds as a biogeochemically important process mediating concomitant turnover of sulfur, nitrogen, and carbon. We used a newly developed approach consisting of molecular analyses in stimulation experiments and in situ abundance. The molecular approach was based on single-strand conformational polymorphism (SSCP) analysis of the bacterial community RNA, which allowed identification of potential denitrifiers based on the sequences of enhanced SSCP bands and monitoring of the overall bacterial community during the experiments. Sequences of the SSCP bands of interest were used to design highly specific primers that enabled (i) generation of almost complete 16S rRNA gene sequences using experimental and environmental DNA as templates and (ii) quantification of the bacteria of interest by real-time PCR. By using this approach we identified the bacteria responsible for autotrophic denitrification as a single taxon, an epsilonproteobacterium related to the autotrophic denitrifier Thiomicrospira denitrificans. This finding was confirmed by material balances in the experiments that were consistent with those obtained with continuous cultures of T. denitrificans. The presence and activity of a bacterium that is phylogenetically and physiologically closely related to T. denitrificans could be relevant for the carbon budget of the central Baltic Sea because T. denitrificans exhibits only one-half the efficiency for carbon dioxide fixation per mol of sulfide oxidized and mol of nitrate reduced of Thiobacillus denitrificans hypothesized previously for this function.
Steep redoxclines form between oxic surface water and the stagnant, sulfidic hypolimnion in the e... more Steep redoxclines form between oxic surface water and the stagnant, sulfidic hypolimnion in the eutrophied, brackish water Baltic Sea. Nitrification, denitrification, and anammox were measured at and below the redoxcline to quantify the role of water-column nitrogen processes in the overall magnitude of nitrogen removal in the Baltic Sea. Rates of nitrification were very high (up to 85 nmol N L 21 d 21 ) at the oxic-anoxic interface, but, surprisingly, nitrification was separated from the processes reducing nitrate to N 2 (up to 810 nmol N L 21 d 21 ) by tens of meters in depth. N 2 production was dominated by chemolithotrophic denitrification, with anammox playing only a negligible role, and limited to the water layers in which nitrite or nitrate coexisted with sulfide. The alternating oxygen concentrations in the basin induce irregular bursts of nitrogen removal. Nitrification takes place after mixing of ammonium-rich deep water with oxic water, and denitrification uses the formed nitrite and nitrate once anoxic conditions re-establish. Although removal rates can be high, conditions allowing such rates are likely short-lived. While the sedimentary denitrification rates at the shallower, oxic areas are lower, they are more constant in time, highlighting the need to avoid hypoxia, which would prevent sedimentary denitrification.
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Papers by Matthias Labrenz