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Role of chemolithoautotrophic microorganisms involved in nitrogen and sulfur cycling in coastal marine sediments
Lipsewers, Y.A. (2017). Role of chemolithoautotrophic microorganisms involved in nitrogen and sulfur cycling in coastal marine sediments. PhD Thesis. [S.n.]: [s.l.]. ISBN 978-90-6266-4924. 225 pp.

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Document type: Dissertation

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  • Lipsewers, Y.A., more

    SummaryThe role of chemolithoautotrophic microorganisms has been considered to be of minor importancein coastal marine sediments although it has not been investigated in depth. Additionally,the impact of seasonal hypoxic/anoxic conditions on microbial chemolithoautotrophy in coastalmarine sediments has not been examined. Therefore, in this thesis the diversity, abundance andactivity of specific groups of chemolithoautotrophic microorganisms involved in the nitrogenand sulfur cycling, as well as the total microbial community, has been determined in coastal sedimentsby using DNA/RNA- and lipid-based biomarker approaches. Results show the presenceand potential importance of chemolithoautotrophs in the biogeochemical cycling of carbon,nitrogen and sulfur. Temporal changes of the diversity, abundance and activity of chemolithoautotrophicmicroorganisms coinciding with seasonal hypoxia in coastal sediments have beendetermined.The diversity, abundance and activity of chemolithoautotrophic microorganisms, such as ammoniaoxidizing archaea (AOA) and bacteria (AOB), anammox and denitrifying bacteria, as wellas sulfate reducing and sulfur oxidizing microorganisms, including sulfide dependent denitrifiers,have been determined. Additionally, the diversity and activity of chemolithoautotrophic microorganismsinvolved in the CBB and rTCA cycle as well as the metabolism of Thaumarchaeotaand the abundance of Archaea have been addressed. In the following studies, we focused oncoastal marine sediments, exposed to summer hypoxia, i.e. (1) the Oyster Grounds in the centralNorth Sea, exposed to decreasing bottom water oxygen concentrations, (2) different sedimenttypes (sand, clay, and mud) of the Iceland Shelf, and (3) seasonally hypoxic and sulfidic sedimentsof saline Lake Grevelingen (The Netherlands).In Oyster Grounds sediments (chapter 2), seasonal variations of archaeal and bacterial ammoniaoxidizers (AOA and AOB) and anammox bacteria, as well as the environmental factorsaffecting these groups, were addressed. We examined the seasonal and depth distribution of theabundance and potential activity of these microbial groups in coastal marine sediments of thesouthern North Sea. We quantified specific intact polar lipids (IPLs) as well as the abundanceand gene expression of their 16S rRNA gene, the ammonia monooxygenase subunit A (amoA)gene of AOA and AOB, and the hydrazine synthase (hzsA) gene of anammox bacteria. AOA,AOB and anammox bacteria were detected and transcriptionally active down to 12 cm sedimentdepth. This study unraveled the coexistence and metabolic activity of AOA, AOB, and anammoxbacteria in bioturbated marine sediments of the North Sea, leading to the conclusion that themetabolism of these microbial groups is spatially coupled based on the rapid consumption ofoxygen that allows the coexistence of aerobic and anaerobic ammonia oxidizers. AOA outnumberedAOB throughout the year which may be caused by the higher oxygen affinity of AOAcompared to AOB. Anammox bacterial abundance and activity were higher during summer,indicating that their growth and activity are favored by higher temperatures and lower oxygenavailable in the sediments due to summer stratifying conditions in the water column. During thesummer, anammox bacteria are probably not in competition with AOA and AOB for ammoniaas the concentrations were relatively high in the sediment pore water most likely as a result ofammonification processes and the activity of denitrifiers and DNRA.In Iceland Shelf sediments (chapter 3), we investigated the activity of Thaumarchaeota insediments by supplying different 13C-labeled substrates which have previously been shown to be184incorporated into archaeal cells in water incubations and/or enrichment cultures. We determinedthe incorporation of 13C-label from bicarbonate, pyruvate, glucose and amino acids into thaumarchaealintact polar lipid-glycerol dibiphytanyl glycerol tetraethers (IPL-GDGTs) during 4–6day incubations of marine sediment cores from three sites on the Iceland Shelf. ThaumarchaealIPLs were present in sediment cores recovered from the Iceland Shelf and the presence of labileIPL-biomarkers for Thaumarchaeota, such as hexose phosphohexose (HPH)-crenarchaeol, suggestedthe presence of living Thaumarchaeota. However, incubations with 13C-labeled substratesbicarbonate, pyruvate, glucose and amino acids did not result in any substantial incorporation ofthe 13C into the biphytanyl chains of these lipids. Turnover times and generation times of thaumarchaeallipids were estimated to be at least several years, suggesting slow growth of sedimentaryThaumarchaeota in contrast to other sedimentary organisms, and/or a slow degradation ofIPL-GDGTs, in contrast to bacterial or eukaryotic PLFAs.In Lake Grevelingen sediments (chapter 4), we evaluated the abundance, diversity and potentialactivity of denitrifying, anammox, and sulfide-dependent denitrifying bacteria in the sedimentsof the seasonally hypoxic saline Lake Grevelingen, known to harbor an active microbialcommunity involved in sulfur oxidation pathways. Depth distributions of 16S rRNA gene, nirSgene of denitrifying and anammox bacteria, aprA gene of sulfur-oxidizing and sulfate-reducingbacteria, and ladderane lipids of anammox bacteria were studied in sediments impacted by seasonallyhypoxic bottom waters. This study unraveled the coexistence and potential activity ofheterotrophic and autotrophic denitrifiers, anammox bacteria as well as SOB/SRB in seasonallyhypoxic and sulfidic sediments of Lake Grevelingen. The nirS-type heterotrophic denitrifierswere a stable community regardless of changes in oxygen and sulfide concentrations in differentseasons and with a similar abundance to that detected in other sediments not exposed to highsulfide concentrations. Besides, nirS-type denitrifiers outnumbered anammox bacteria leadingto the conclusion that anammox does not contribute significantly to the N2 removal processin Lake Grevelingen sediments. The anammox bacteria population seemed to be affected bythe physicochemical conditions between seasons and their abundance and activity was higherin lower sulfide concentrations and low carbon input, also supporting a possible inhibition ofanammox bacteria by sulfide. The sulfide-dependent denitrifiers in Lake Grevelingen sedimentshave proven to be abundant, but their expected sulfide-detoxification potential did not seem toalleviate the predicted inhibition of organoheterotrophic denitrifiers and anammox by sulfide.Both denitrifiers and anammox bacteria activity could be inhibited by the competition with cablebacteria and Beggiatoaceae for electron donors and acceptors (such as sulfide, nitrate and nitrite)before summer hypoxia but might be still supported by the potential sulfide detoxification of thesediment through sulfide oxidation, supporting at least a low activity. During summer hypoxia,sulfide inhibition and low nitrate and nitrite concentrations seem to limit the activity of heterotrophicand autotrophic (sulfide-dependent) denitrifiers and anammox bacteria.Additionally, we examined the changes in activity and structure of the sedimentary chemolithoautotrophicbacterial community in Lake Grevelingen under oxic (spring) and hypoxic(summer) conditions (Chapter 5). Combined 16S rRNA gene amplicon sequencing and analysisof phospholipid derived fatty acids indicated a major temporal shift in community structure.Chemolithoautotrophy rates in the surface sediment were three times higher in spring comparedto summer. Besides, the depth distribution of chemolithoautotrophy was linked to the distinctsulfur oxidation mechanisms identified through microsensor profiling, i.e., canonical sulfur ox189idation, electrogenic sulfur oxidation by cable bacteria, and sulfide oxidation coupled to nitratereduction by Beggiatoaceae. The metabolic diversity of the sulfur-oxidizing bacterial communitysuggests a complex niche partitioning within the sediment probably driven by the availability ofreduced sulfur compounds and electron acceptors regulated by seasonal hypoxia.In Lake Grevelingen sediments, we also compared the archaeal abundance and compositionby DNA-based methods and the archaeal intact polar lipid (IPL) diversity in surface sedimentsto determine the potential biological sources of the archaeal IPLs detected in surface sedimentsunder changing environmental conditions (Chapter 6). We observed a dramatic changein the archaeal community composition and lipid abundance in surface sediments of a seasonallyhypoxic marine lake which corresponded to a switch from a Thaumarchaeota-dominatedto a DPANN-dominated archaeal community, while the total IPLs detected were significantlyreduced. Considering the reduced genome of the members of the superphylum DPANN andtheir apparent inability to synthesize their own membrane lipids, we hypothesize that they usethe CLs previously synthesized by the Thaumarchaeota to form their membrane. Results indicatean active recycling of fossil IPLs in the marine surface sediment.Overall, the research presented in this thesis has provided new insights on the diversity, abundanceand activity of chemolithoautotrophic microorganisms, such as AOA, AOB, anammoxand denitrifying bacteria, as well as sulfate reducing and sulfur oxidizing microorganisms, includingsulfide-dependent denitrifiers in coastal marine sediments. Hypoxia and increasing sulfideconcentration have proven to be key factors restricting the presence and activity of the abovementioned groups. In addition, the interactions with other microbial groups and bioturbationseem to favor the presence of specific chemolithoautotrophs in unexpected sediment depths,such as the presence of AOA in depths where the oxygen concentration was expected to beundetectable, or the presence of anammox bacteria in bioturbated sediments where nitrate reducerscould thrive and provide nitrite to fuel the anammox process.

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