Thaumarchaeota in Marine Sediments

Marine sediments host the largest reservoir of organic carbon in the world as well as a huge number of microorganisms. These complex microbial communities and their associated metabolic activities have a profound impact onglobal biogeochemical cycles. Understanding their structure and function is crucial for predicting the fate of carbon and other essential elements in the marine system. However, the vast majority of subsurface microorganisms are poorly characterized and their physiological activities remain unknown. One of the most widespread and abundant microbial groups in oceanic sediments are thaumarchaeota, a phylum of archaea formerly referred to as mesophilic crenarchaeota.

Thaumarchaeota in aerobic environments, i.e. in the oceanic plankton and in soils and freshwater are capable of aerobic ammonia oxidation and therefore contribute to global nitrogen cycling by performing the first step in nitrification. While the metabolism of thaumarchaeota in marine sediments is unknown, their metabolic activities are expected to be different and probably more versatile since they reside in large numbers in anaerobic horizons of the deep sediments. this study we will investigate the genomic potential of different thaumarchaeotal clades that typically occur in marine sediments and we will also attempt to cultivate and physiologically characterize representatives of them. Our study builds on an earlier intense investigation of two highly stratified marine sediment cores from the ultra-slow spreading ridge of the North Atlantic (PNAS 2012, 109(42):E2846-55). The 3 m cores exhibited an unusually strong and compressed geochemical layering allowing us to find quantitative correlations between the sediment geochemistry and changes in the microbial communities. Eight out of 15 horizons in these cores were dominated by thaumarchaeota of various subclades typical for deep marine sediments. Samples from these horizons will be used in this project to directly extract DNA for metagenomic investigations and to extract cells for cell sorting and subsequent single cell genomics. In parallel we will set up a variety of enrichments based on the geochemical context data available. Along the project, genomic information will feed into the cultivation strategies and enrichment cultures will in turn be used as starting material for single cell genomics. In addition isotopic studies on actively growing archaeal enrichments will be performed using NanoSIMS imaging (nano secondary ion mass spectrometry) to investigate the assimilation of substrates by certain archaeal clades. Comparative genomic studies of thaumarchaeota from marine sediments will be performed to tackle their specific genomic and physiological adaptations and their evolutionary relationship with other thaumarchaeota and related archaeal clades.

Our study will provide insights into the physiological and metabolic potential, genetic setup and evolution of one of the most widespread and abundant, but very little studied microbial groups on this planet.

Duration: 01.08.2014-31.07.2019

Funding agency: Austrian Science Fund (FWF): P 27017

Project leader: Prof. Christa Schleper

Participants: Christa Schleper, Sophie Abby, Michael Melcher, Ziga Zebec, Chris Pruckner, Tilman Schmider

Summary of final report

Marine sediments host the largest reservoir of organic carbon in the world as well as a hugenumber of microorganisms. These complex microbial communities and their associatedmetabolic activities have a profound impact on global biogeochemical cycles. Understandingtheir structure and function is crucial for predicting the fate of carbon and other essentialelements in the marine system. Yet, relatively little is known about the activity andadaptations of these microorganisms. In this project we have reconstructed the genomes ofarchaea from the phylum Thaumarchaeota which are abundant in deep sea sediments. Weanalyzed samples from the ultra slow spreading ridge in the North Atlantic and from theabyssal plains, i.e. some of the deepest spots in the Pacific Ocean. The eleven reconstructedgenomes give information about three different clades that evolved independently, probablyfrom marine and shallow sediment ancestors, respectively. They are all capable of ammoniaoxidation like their relatives from marine pelagic oceans and shallow sediments, freshwateror soil. However, they show specific metabolic adaptations and repair mechanisms that allowthem to cope with the extreme conditions of the deep ocean, in particular nutrient limitationand high hydrostatic pressure. This includes the capacity to scavenge fermentation productsand amino acids from the environment which might support them in saving metabolic energy,and simultaneously implicate them in the global carbon pool turnover in previouslyundetected ways. In addition, specific capacities to maintain intracellular ion concentrationsand extra genes for repair of their genetic material allows these organisms to thrive in suchextreme deep sea environments. By reconstructing the ancestors of the different ammoniaoxidizing lineages of thaumarchaeota, we demonstrate that this group evolved from anaerobic ancestor in hot springs and by adaptative radiation formed an impressivelywidespread microbial clade on Earth with all organisms thriving from the same energymetabolism, i.e. by oxidizing ammonia to nitrite and fixing inorganic carbon thus contributingto the nitrogen and carbon cycling on global scales.

Peer-reviewed publications related to or funded through this project

  • Abby S, Kerou M, Schleper C. (2020) Ancestral reconstructions decipher majoradaptations of ammonia oxidizing archaea upon radiation into moderate terrestrialand marine environments. BioRxiv: 176255.
  • Kerou M, Ponce-Toledo R, Zhao R, Abby S, Hirai M, Nomaki H, Takaki Y, Nunoura T,Jorgensen J, Schleper C. (2020) Genomes of Thaumarchaeota from deep seasediments reveal specific adaptations of three independently evolved lineages. BioRxiv: 168906
  • Spang A, Saw JH, Jørgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE, vanEijk R, Schleper C, Guy L, Ettema TJ (2015) Complex archaea that bridge the gapbetween prokaryotes and eukaryotes. Nature 521(7551): 173-179. doi:10.1038/nature14447.
  • Abby SS, M Melcher, M Kerou, M Krupovic, M Stieglmeier, C Rossel, C Schleper (2018) Candidatus Nitrosocaldus cavascurensis, an ammonia oxidizing, extremely thermophilic archaeon with a highly mobile genome. Frontiers in microbiology 9: 28. Doi: 10.3389/fmicb.2018.00028
  • Alves RJE, Minh BQ, Urich T, von Haeseler A, Schleper C. (2018) Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes. Nat Commun 9: 1517. Doi: 10.1038/s41467-018-03861-1 
  • Alves RJE, Kerou M, Zappe A, Bittner R, Abby SS, Schmidt H, Pfeifer K, Schleper C. (2019) Ammonia oxidation by the arctic terrestrial thaumarchaeote Ca. Nitrosocosmicus arcticus is stimulated by increasing temperatures. Frontiers in microbiology 10: 1571. DOI: 10.3389/fmicb.2019.01571
  • Elling FJ, Könneke M, Nicol GW, Stieglmeier M, Bayer B, Spieck E, Schleper C, Hinrichs KU. (2017) Chemotaxonomic characterisation of the thaumarchaeal lipidome. Environmental Microbiology 19 (7): 2681-2700. DOI: 10.1111/1462-2920.13759
  • Kerou M, Schleper C (2016) Genus Nitrososphaera. In: Bergey’s Manual ofSystematics of Archaea and Bacteria. William B. Whitman (ed.). Wiley Online Library. Doi: 10.1002/9781118960608.gbm01294.
  • Kerou M, Alves RJE, Schleper C (2016) Class Nitrososphaeria In: Bergey’s Manual of Systematics of Archaea and Bacteria. William B. Whitman (ed.). Wiley Online Library. Doi: 10.1002/9781118960608.cbm00055.
  • Kerou M, Schleper C (2016) Family Nitrososphaeraceae. In: Bergey’s Manual of Systematics of Archaea and Bacteria. William B. Whitman (ed.). Wiley Online Library. Doi: 10.1002/9781118960608.fbm00265.
  • Jung MY, Kim JG, Sinninghe Damsté JS, Rijpstra WI, Madsen EL, Kim SJ, Hong H, Si OJ, Kerou M, Schleper C, Rhee SK. (2016) A hydrophobic ammonia‐oxidizing archaeon of the Nitrosocosmicus clade isolated from coal tar‐contaminated sediment. Environmental microbiology reports 8 (6): 983-992. Doi: 10.1111/1758-2229.12477 
  • JA Kozlowski, M Stieglmeier, C Schleper, MG Klotz, LY Stein (2016) Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota. The ISME journal 10 (8): 1836-1845. Doi: 10.1038/ismej.2016.2
  • Bayer B, Vojvoda J, Offre P, Alves RJ, Elisabeth NH, Garcia JA, Volland JM, Srivastava A, Schleper C, Herndl GJ. (2016) Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation. The ISME journal 10 (5): 1051-1063. Doi: 10.1038/ismej.2015.200
  • Kerou M, Offre P, Valledor L, Abby SS, Melcher M, Nagler M, Weckwerth W, Schleper C. (2016) Proteomics and comparative genomics of Nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers. Proceedings of the National Academy of Sciences 113 (49): E7937-E7946. Doi: 10.1073/pnas.1601212113