Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages

Abstract

26Marine sediments represent a vast habitat for complex microbiomes. Among these, ammonia oxidizing 27 archaea (AOA) of the phylum Thaumarchaeota are one of the most common, yet little explored 28 inhabitants, that seem extraordinarily well adapted to the harsh conditions of the subsurface biosphere. 29We present 11 metagenome-assembled genomes of the most abundant AOA clades from sediment cores 30 obtained from the Atlantic Mid-Ocean ridge flanks and Pacific abyssal plains. Their phylogenomic 31 placement reveals three independently evolved clades within the order Ca. Nitrosopumilales, of which 32 no cultured representative is known yet. In addition to the gene sets for ammonia oxidation and carbon 33 fixation known from other AOA, all genomes encode an extended capacity for the conversion of 34 fermentation products that can be channeled into the central carbon metabolism, as well as uptake of 35 amino acids probably for protein maintenance or as an ammonia source. Two lineages encode an additional (V-type) ATPase and a large repertoire of gene repair systems that may allow to overcome 37 challenges of high hydrostatic pressure. We suggest that the adaptive radiation of AOA into marine 38 sediments occurred more than once in evolution and resulted in three distinct lineages with particular 39 adaptations to this extremely energy limiting and high-pressure environment. 40 41 42 Introduction 43 44 Ammonia oxidizing archaea (AOA) comprise one of the most successful archaeal phyla having 45 colonized almost every imaginable oxic environment of the planet where they emerge as key players in 46 the nitrogen cycle [1-6]. This includes the marine environment where they dominate archaeal 47 communities associated with oxic sediments ranging from shallow estuaries to the open ocean [7-12], 48and from the surface layers all the way into the deep oceanic crust [13][14][15]. In these ecosystems they 49 seem to play a critical role in the transformation of nitrogen compounds and control its partitioning into 50 the bottom ocean and the underlying oceanic crust [12,[14][15][16][17][18][19]). 52Studies from the North Atlantic and Pacific show that the composition of the sedimentary AOA 53 population differs drastically from that in the overlying water suggesting distinct ecophysiological 54 potential to colonise sedimentary environments, albeit all were found to belong to the order 55 Nitrosopumilales (NP) [20]. Whereas the amoA-NP-gamma clade seems to be dominant and 56 omnipresent in these oceans, irrespective of water depths, the amoA-NP-alpha clade represents the most 57 abundant ecotypes in deep ocean waters [6, 7,[21][22][23][24][25][26][27] (nomenclature based amoA gene classification 58 [28]). In contrast, dominant phylotypes in deep-sea sediments belong to the amoA-NP-theta and amoA-59 NP-delta clades [11, 12]. In addition, in cases of oligotrophic oceanic regions, these were detected 60 throughout the sediment column and further into the underlying basaltic crust, even at depth where 61 oxygen is below detection [7, ...

Geochemical transition zone powering microbial growth in subsurface sediments

“…Although low abundances of ammonia-oxidizing archaea were also observed in sediments below the oxic zone ( SI Appendix , Fig. S4 ), they have no known genetic machinery to use alternative electron acceptors other than O 2 ( 49 ), questioning their contributions to nitrite production in the anoxic NATZ. Instead, we found a variety of periplasmic nitrate reductase alpha subunit (NarG) sequences affiliated with Planctomycetes, Heimdallarchaeota, Cytophagales (Bacteroidetes phylum), and Solirubrobacterales (Actinobacteria phylum) in the metagenome assembly of the NATZ of GC08 ( SI Appendix , Fig.…”

Limited accessibility of nitrogen supplied as amino acids, amides, and amines as energy sources for marine Thaumarchaeota

“…If excess glutamine is transported into thaumarchaeal cells, some may be recycled to NH 4 + for either assimilatory or dissimilatory use. This amino acid “recycling” is common in energy-starved microbes (Lever et al ., 2015) and was recently hypothesized to play a role in thaumarchaeal survival in deep sea sediments (Kerou et al ., 2021). It is possible that energy-starved Thaumarchaeota in our experiment transported glutamine into their cells but were unable to incorporate it into biomass, so they hydrolyzed the glutamine amide N and shunted the resulting NH 4 + into energy production, leading to slow growth.…”

Analysis of biomass productivity and physiology of Nitrososphaera viennensis grown in continuous culture

“…Since then multiple isolates and enrichments of ammonia oxidizing archaea (AOA) have been established and characterized to further improve our understanding of these ubiquitously abundant organisms (De La Torre et al, 2008;Blainey et al, 2011;Lehtovirta-Morley et al, 2011Lebedeva et al, 2013;Jung et al, 2014;Zhalnina et al, 2014;Santoro et al, 2015;Qin et al, 2017;Sauder et al, 2017Sauder et al, , 2018Abby et al, 2018;Daebeler et al, 2018;Alves et al, 2019;Bayer et al, 2019;Nakagawa et al, 2021). Viable habitats include oceanic crust (Nunoura et al, 2013;Jørgensen and Zhao, 2016;Zhao et al, 2020), deep sea sediments (Francis et al, 2005;Park et al, 2008;Nunoura et al, 2018;Vuillemin et al, 2019;Zhao et al, 2019;Kerou et al, 2021), marine water column (Qin et al, 2017;Bayer et al, 2019;Santoro, 2019), oxygen minimum zones (Bristow et al, 2016), various kinds of soils (Lehtovirta-Morley et al, 2011Tourna et al, 2011;Jung et al, 2014;Zhalnina et al, 2014;Alves et al, 2019), fresh water ecosystems (French et al, 2012(French et al, , 2021Sauder et al, 2018), waste water treatment plants (Mußmann et al, 2011;Sauder et al, 2017), terrestrial hot springs (De La Torre et ...…”