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Bacterial chemoautotrophy in coastal sediments
Vasquez-Cardenas, D. (2016). Bacterial chemoautotrophy in coastal sediments. PhD Thesis. UvA: Amsterdam. ISBN 978-94-91407-33-8. 215 pp. hdl.handle.net/11245/1.531841

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Document type: Dissertation

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  • Vasquez-Cardenas, D., more

Abstract
    Chemoautotrophy is the process by which micro-organisms fix CO2 by obtainingenergy from the oxidation of reduced compounds such sulfide and ammonium (e.g.sulfur oxidation and nitrification). This metabolism is widespread in nature and isvastly studied in extreme environments such as hydrothermal vents and chemoclinesin hypoxic basins where it contributes greatly to primary production. However, chemoautotrophsare easily overlooked in coastal areas where the photoautotrophicorganisms are the main primary producers. Moreover, chemoautotrophs are estimatedto have CO2 fixation efficiencies of less than 10% (i.e., the ratio of chemoautotrophicCO2 fixation over the total CO2 released from the mineralization of organic matter),which results in the exclusion of chemoautotrophic carbon production from coastalcarbon budgets. Nonetheless, the production of sulfide (the main electron donor forchemoautotrophic bacteria in sediments) is much higher in coastal sediments thanin hydrothermal vent systems, which suggests a greater potential for chemoautotrophicsulfur oxidizers in coastal sediments. In fact, chemoautotrophs have been shown tofix up to 22% of the carbon respired in subtidal sediments, and sulfur oxidation bylarge filamentous bacteria (Beggiatoaceae) can account for up to 90% of the oxygenrespiration in sediments with overlapping O2 and H2S. Thus the aim of this thesiswas to assess chemoautotrophic activity in a range of coastal environments by identifyingpotential key players, determining regulatory factors of the process and evaluatingthe importance of chemoautotrophic activity in coastal ocean sediments.The majority of chemoautotrophic bacteria identified through sequencing (16SrRNA gene and 16S rRNA, and carboxylation genes of two carbon fixation pathways:the Calvin Benson-Bassham and the reductive tricarboxylic acid cycles) wasrelated to sulfur oxidizing bacteria, from the Gamma-, Epsilon- and Deltaproteobacteriaclades (Chapters 2, 3, 4). The co-occurrence of these diverse groups ofsulfur-oxidizing chemoautotrophic bacteria may be attributed to a complex nichedifferentiation driven most likely by the availability of different sulfur species (freesulfide, iron sulfide, thiosulfate, elemental sulfur) in the different sediment types. Forexample, filamentous Beggiatoaceae (Gammaproteobacteria) are characteristic forcohesive, sulfur-rich sediments because they have a high affinity for H2S and highuptake rates that allow them to compete with chemical sulfide oxidation at O2-H2S interfaces (Chapter 2). Furthermore, vacuolated Beggiatoaceae can outcompete othersulfur-oxidizers because they are capable of storing nitrate intracellularly and oxidizingsulfide to sulfate in two spatially separated reactions (Chapter 4). Metabolicallyversatile Epsilonproteobacteria were also found in this sediment type where theyprobably oxidize elemental sulfur aerobically or with nitrate. The research describedin this thesis suggests that these Epsilonproteobacteria may depend on the activityof filamentous sulfur oxidizers such as vacuolated-Beggiatoaceae and heterotrophiccable bacteria (Chapter 3, 4). Unicellular, sulfur-oxidizing Gammaproteobacteriaalso appear to be metabolically linked to cable bacteria in cohesive sediments butthe exact mechanism remains elusive (Chapter 3, 4). In contrast, in bioturbated sedimentsunicellular Gammaproteobacteria potentially use iron sulfide as their mainelectron donor (Chapter 2). Lastly, chemoautotrophic Deltaproteobacteria relatedto sulfate reducers that can disproportionate sulfur were prevalent in deeper anoxicsediment layers and during hypoxic bottom water conditions (Chapter 2, 4).Rates of bacterial dark carbon fixation by bacteria were surveyed in a variety ofcoastal sediments covering intertidal flats, a marine lake, nearshore and continentalshelf sediments by means of stable isotope probing (¹³C-DIC) and bacterial biomarkeranalysis (phospholipid derived fatty acids, PLFA-SIP). In total we report 26 newobservations that more than quadruple the existing number (6) of sedimentary chemoautotrophyrates available in the literature. Dark carbon fixation rates rangedfrom 0.07 to 36 mmol C m¯² d¯¹ with highest activity found in cohesive salt marshsediments, while lowest rates were found in advective-driven continental shelf sediments.The majority of the dark carbon fixation rates (n=17) fell within 1 and 10mmol C m¯² d¯¹. A correlation analysis to determine possible environmental factorsthat influence the dark carbon fixation rate resulted in a significant power-law correlationbetween chemoautotrophy rates and the benthic oxygen consumption (Chapter6). This correlation indicates that as benthic oxygen consumption increases, darkcarbon fixation increases more than proportionally with the highest values towardsshallower water depth. Using the sediment oxygen uptake rate as a proxy for sedimentmineralization we were able to estimate the CO2 fixation efficiency for thedifferent sediments. Across the dataset, we found a CO2 fixation efficiency rangingfrom 0.01 to 0.32 with a median of ~0.06, which corresponds well with the CO2fixation efficiency of 0.07 that has been estimated for coastal sediments based onsimplified electron balance calculations. When differentiating between three depthzones in the coastal ocean, we found 3% CO2 fixation efficiency in continental shelfsediments (50-200 m water depth), 9% for nearshore sediments (0-50 m water depth,including intertidal sediments), and 21% for salt marshes (Chapter 6). Thus, chemoautotrophicactivity plays a more prevalent role in the carbon cycling in reactiveintertidal sediments (especially in salt marshes) than in deeper continental shelf sediments. With these mean CO2 fixation efficiencies for the different water depthswe estimated for coastal sediments a global chemoautotrophic production of 0.06Pg C y¯¹ (Chapter 6). This is two-and-a-half times lower than the conservative estimateof 0.15 Pg C y¯¹ indicating that previous studies have severely overestimatedthe contribution of chemoautotrophy in coastal sediments.Furthermore, five distinct depth-distribution patterns of chemoautotrophy aredescribed that could be linked to three sediment types that differ in the main modeof pore water transport: advective, bioturbated, and diffusive, which align well withsediment characteristics such as grain size, porosity, organic matter content and faunaactivity (Chapter 6). In the case of diffusive sediments, the prevalent mode of sulfuroxidation was used to distinguish between three additional categories: electrogenicsulfur oxidation by cable bacteria, sulfide by motile, nitrate accumulating Beggiatoaceaeand canonical sulfide oxidation within an overlapping O2-H2S interface. (1)Sediments with canonical sulfide oxidation had most of the chemoautotrophic activityat the sediment surface where electron donor (H2S) and acceptor (O2 or NO3¯) overlap(Chapters 2, 3, 4). (2) Nitrate-storing Beggiatoaceae create a suboxic zone in thesediment by gliding up and down between the surface and the sulfide horizon depth.In this scenario Beggiatoa is the main contributor to chemoautotrophic activity, whichis found at the surface and throughout the suboxic zone (Chapter 4). (3) Electrogenicsulfur oxidation by cable bacteria also creates a suboxic zone in sediments but has adistinct pH profile, which distinguishes it from that of the nitrate-storing Beggiatoaceae.In this case, dark carbon fixation is evenly distributed from the surface tobelow the sulfide horizon potentially by means of a sulfur-oxidizing consortiumbetween chemoautotrophic bacteria and the heterotrophic cable bacteria (Chapters3, 4). (4) Bioturbating activity results in the intrusion of electron acceptors into deepanoxic sediments via intense bio-irrigation whereas strong particle mixing supportsiron cycling. Thus chemoautotrophic activity is enhanced in deeper sediments andalong the burrow walls, as well as at the surface compared to non-bioturbating sediments(Chapter 5, 6). Moreover, the effects of bioturbation on chemoautotrophicbacteria are species-specific and thus vary between sites with differing macrofaunalcommunities (Chapter 5). (5) In advective-driven permeable sediments, the constantflushing of the sediment produces deep oxygen penetration which enhances aerobicrespiration that favors nitrifying bacteria with low growth yields (0.10), but diminishesanaerobic sulfate reduction and thus sulfide oxidation. This results in a minimumchemoautotrophic activity throughout the sediment matrix (Chapter 6).In accordance with the three main objectives of this thesis it is concluded that 1)chemoautotrophy in coastal sediments is conducted by a diverse group of sulfur-oxidizingbacteria which co-occur either through complex sulfur-niche differentiation inbioturbated sediments or by way of a bacterial consortium when filamentous sulfuroxidizers are present in diffusive sediments, but the exact mechanisms involved remainto be determined. 2) Chemoautotrophy rates vary depending on the main mode ofpore water transport, which affects the sediment mineralization rate and the availabilityof electron donors and acceptors. Five distinct depth-distribution patterns of the darkcarbon fixation are described that are linked to the main mode of sulfur oxidation. 3)Globally, chemoautotrophic production is one order of magnitude higher than thatfound in hydrothermal vents where chemoautotrophic bacteria are responsible for mostof the primary production. Coastal benthic chemoautotrophy may therefore be animportant source of renewed labile organic matter, especially in intertidal sediments,which should not be overlooked in future food web and biogeochemical studies.

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