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Primary Production in the Water Column As Major Structuring Hindawi Archaea Volume 2019, Article ID 3717239, 12 pages https://doi.org/10.1155/2019/3717239 Research Article Primary Production in the Water Column as Major Structuring Element of the Biogeographical Distribution and Function of Archaea in Deep-Sea Sediments of the Central Pacific Ocean Franziska Wemheuer ,1,2 Avril Jean Elisabeth von Hoyningen-Huene ,1 Marion Pohlner,3 Julius Degenhardt,3 Bert Engelen,3 Rolf Daniel,1 and Bernd Wemheuer 1,4 1Genomic and Applied Microbiology and Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, University of Göttingen, Göttingen, Germany 2Applied Marine and Estuarine Ecology, Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, Australia 3Paleomicrobiology Group, Institute for Chemistry and Biology of the Marine Environment, University of Oldenburg, Oldenburg, Germany 4Centre for Marine Bio-Innovation, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, Australia Correspondence should be addressed to Bernd Wemheuer; [email protected] Received 31 July 2018; Revised 4 December 2018; Accepted 8 January 2019; Published 3 March 2019 Academic Editor: Stefan Spring Copyright © 2019 Franziska Wemheuer et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Information on environmental conditions shaping archaeal communities thriving at the seafloor of the central Pacific Ocean is limited. The present study was conducted to investigate the diversity, composition, and function of both entire and potentially ° active archaeal communities within Pacific deep-sea sediments. For this purpose, sediment samples were taken along the 180 meridian of the central Pacific Ocean. Community composition and diversity were assessed by Illumina tag sequencing targeting archaeal 16S rRNA genes and transcripts. Archaeal communities were dominated by Candidatus Nitrosopumilus (Thaumarchaeota) and other members of the Nitrosopumilaceae (Thaumarchaeota), but higher relative abundances of the Marine Group II (Euryarchaeota) were observed in the active compared to the entire archaeal community. The composition of the entire and the active archaeal communities was strongly linked to primary production (chlorophyll content), explaining more than 40% of the variance. Furthermore, we found a strong correlation of the entire archaeal community composition to latitude and silicic acid content, while the active community was significantly correlated with primary production and ferric oxide content. We predicted functional profiles from 16S rRNA data to assess archaeal community functions. Latitude was significantly correlated with functional profiles of the entire community, whereas those of the active community were significantly correlated with nitrate and chlorophyll content. The results of the present study provide first insights into benthic archaeal communities in the Pacific Ocean and environmental conditions shaping their diversity, distribution, and function. Additionally, they might serve as a template for further studies investigating archaea colonizing deep-sea sediments. 1. Introduction marine (deep-sea) sediments [10–12]. Deep-sea sediments constitute one of the largest ecosystems on earth, covering Archaea play a key role in global biogeochemical cycles [1–4]. approximately 65% of its surface. This ecosystem is charac- These microorganisms are widely distributed in various envi- terized by extreme conditions including high pressure, cold ronments such as permafrost [5], hot springs [6, 7], hypersa- temperatures, and lack of light. Nonetheless, deep-sea sedi- line lakes [8], marine seawaters [9], and freshwater as well as ments harbor taxonomically and metabolically diverse 2 Archaea archaeal communities [11–16]. These communities are gen- CTD-rosette equipped with a fluorometer (FluoroWetla- erally dominated by archaeal taxa belonging to the phyla bECO_AFL_FL, SN: FLNTURTD-4111). Data were recorded Thaumarchaeota and Euryarchaeota [11, 13, 16–18]. and stored using the standard software Seasave V 7.23.2 and Given the important ecological role of Archaea, it is fun- processed using ManageCTD. The sum of chlorophyll con- damental to decipher key drivers of diversity, distribution, centrations measured in the top 500 m of the water column and function of archaeal communities in marine deep-sea was used as a measure for the primary productivity in sediments. Previous investigations revealed that these com- the water column at the different sampling sites. Raw data munities are affected by a wide range of environmental con- are available at PANGAEA: https://doi.pangaea.de/10.1594/ ditions. These include sediment depth, distance from land, PANGAEA.864673 [24]. water depth, site, and latitude [12–15, 19]. Other important The geochemical analysis of pore water and bulk sedi- factors driving archaeal communities in marine sediments ments for all sites was described previously [22]. In brief, sed- are the hydrography of overlying water masses and/or the iments were freeze-dried (Beta 1-8 LDplus, Christ, Germany) quantity and composition of organic matter [11, 13, 20]. and homogenized using a Mixer Mill MM 400 (3 Hz, 50 min; For example, Sorensen and Teske [14] investigated the active Retsch, Germany). Total carbon (TC) and sulfur (S) content archaeal community in deep marine subsurface sediments were measured with an elemental analyzer (Eltra CS-800, from the Peru Margin and observed changes in activity and Germany) with a precision and accuracy of <3% (1σ). Inor- community composition over short distances in geochemi- ganic carbon (IC) was analyzed using an acidification module cally distinct zones. In another study on prokaryotic commu- (Eltra CS-580). The content of total organic carbon (TOC) ° nities in deep-sea sediments collected at latitudes of 34 Nto was calculated by difference (TC – IC). Major and trace element ° 79 N, archaeal abundances significantly increased from mid- analysis in sediments were performed by wavelength-dispersive dle to high latitudes [13]. X-ray fluorescence (XRF; Panalytical AXIOS plus). Nutrient Despite the increasing number of studies, our knowledge concentrations of ammonium (NH4), nitrate (NO3), phosphate of archaeal communities in deep-sea sediments of the cen- (PO4), and silicic acid in porewaters were determined photo- tral Pacific Ocean is still very limited. In this study, we metrically using the Multiskan GO Microplate Spectropho- assessed entire and potentially active archaeal communities tometer (Thermo Fisher Scientific, USA). The method for at the seafloor of the Pacific Ocean. Sediments were sampled measuring ammonium was modified after Benesch and Man- in the central Pacific during RV Sonne expedition SO248 gelsdorf [25]. Nitrate was quantified with the method ° along the 180 meridian. Sediment samples (0-1 cm below described by Schnetger and Lehners [26]. Concentrations of ° seafloor, cmbsf) were collected at nine sites from 27 Sto phosphate and silicic acid were determined following the ° 59 N exhibiting different depths of 3,258 to 5,909 meters protocol of Grasshoff et al. [27]. All measured environmental below sea level (mbsl). properties are provided in Supplementary Table S1. Entire and potentially active archaeal communities were assessed by Illumina tag sequencing of 16S rRNA amplicons generated from 16S rRNA genes and transcripts amplified by 2.3. Nucleic Acid Extraction and Sequencing. DNA extraction PCR and RT-PCR, respectively. In addition, functional pro- from sediment samples was performed using the DNeasy fi fi PowerSoil Kit (Qiagen, Germany) according to the manufac- les (arti cial metagenomes) were predicted using Tax4Fun2 ’ [21] to investigate functional changes of archaeal communi- turer s instructions. RNA was extracted using the AllPrep fi DNA/RNA Mini Kit (Qiagen) following the manufacturer’s ties. The transpaci c survey is of fundamental interest as it fi offers the opportunity to assess archaeal diversity, commu- protocol with some modi cations as described previously nity composition, and its function in deep-sea sediments [22]. The concentration and purity of DNA and RNA exhibiting a wide range of environmental conditions. extracts were determined spectrophotometrically (Nano- Drop 2000c; Thermo Fisher Scientific, USA). Entire and potentially active archaeal communities were 2. Material and Methods assessed by Illumina tag sequencing of 16S rRNA amplicons fi 2.1. Origin and Sampling of Sediments. Sediment samples generated from 16S rRNA genes and transcripts ampli ed by were collected as described previously [22] in May 2016 dur- PCR and RT-PCR, respectively. For RNA analysis, residual DNA was removed from extracted RNA by Turbo DNAse ing RV Sonne expedition SO248 along a transect ranging from fi Auckland, New Zealand, to Dutch Harbor, Alaska, USA treatment, and the absence of DNA was con rmed by PCR (Figure 1, Supplementary Table S1). Briefly, sediment cores using universal primers as described by Schneider et al. were taken using a multicorer (Octopus, Germany) at nine [28]. Subsequently, cDNA was generated from DNA-free sites, exhibiting water depths between 3,258 and 5,909 mbsl. RNA using the SuperScript III reverse transcriptase (Thermo ff Fisher Scientific) according to Wemheuer et al. [29] using the Sediment samples were collected using sterile, cuto ′ syringes and rhizons
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