Patterns of thaumarchaeal gene expression in culture and diverse marine environments

135

Summary Marine sponges represent one of the few eukaryotic groups that frequently harbour symbiotic members of the Thaumarchaeota, which are important chemoautotrophic ammonia‐oxidizers in many environments. However, in most studies, direct demonstration of ammonia‐oxidation by these archaea within sponges is lacking, and little is known about sponge‐specific adaptations of ammonia‐oxidizing archaea (AOA). Here, we characterized the thaumarchaeal symbiont of the marine sponge Ianthella basta using metaproteogenomics, fluorescence in situ hybridization, qPCR and isotope‐based functional assays. ‘Candidatus Nitrosospongia ianthellae’ is only distantly related to cultured AOA. It is an abundant symbiont that is solely responsible for nitrite formation from ammonia in I. basta that surprisingly does not harbour nitrite‐oxidizing microbes. Furthermore, this AOA is equipped with an expanded set of extracellular subtilisin‐like proteases, a metalloprotease unique among archaea, as well as a putative branched‐chain amino acid ABC transporter. This repertoire is strongly indicative of a mixotrophic lifestyle and is (with slight variations) also found in other sponge‐associated, but not in free‐living AOA. We predict that this feature as well as an expanded and unique set of secreted serpins (protease inhibitors), a unique array of eukaryotic‐like proteins, and a DNA‐phosporothioation system, represent important adaptations of AOA to life within these ancient filter‐feeding animals.

Section: Resultssupporting

confidence: 53%

Characterization of a thaumarchaeal symbiont that drives incomplete nitrification in the tropical spongeIanthella basta

Moeller

Webster

Herbold

et al. 2019

135

“…), suggesting a coupled expression of these two genes that corroborates the findings of Carini et al . (). Deviations from an ideal 1:1 ratio between normalized transcript abundances likely results from differential physiological or environmental controls on the expression of amoA and nirK , as well as variations in per‐genome copy numbers as described previously.…”

Section: Resultsmentioning

confidence: 98%

“…Another functional gene that has been proposed as an alternative molecular marker for Thaumarchaeota is the copper‐containing nitrite reductase gene ( nirK ) (Bartossek et al ., ; Lund et al ., ), which is prominent among the candidate genes proposed to be involved in archaeal ammonia oxidation (Stahl and de la Torre, ; Kerou et al ., ; Kozlowski et al ., ; Tolar et al ., ; Carini et al ., ). Several models have been proposed incorporating NirK into the core ammonia oxidation pathway: in one, NirK catalyses the oxidation of either NH 2 OH to NO, or NO to NO 2 − (Carini et al ., ). In another proposed model, two molecules of NO 2 − are generated from NH 2 OH and NO, and NirK is proposed to reduce one of these NO 2 − molecules back into NO, returning it to the NO 2 − ‐generation module (Kozlowski et al ., ).…”

Section: Introductionmentioning

confidence: 97%

See 1 more Smart Citation

Depth distributions of nitrite reductase (nirK) gene variants reveal spatial dynamics of thaumarchaeal ecotype populations in coastal Monterey Bay

Reji

Tolar

Smith

et al. 2019

Summary Ammonia‐oxidizing archaea (AOA) of the phylum Thaumarchaeota are key players in nutrient cycling, yet large gaps remain in our understanding of their ecology and metabolism. Despite multiple lines of evidence pointing to a central role for copper‐containing nitrite reductase (NirK) in AOA metabolism, the thaumarchaeal nirK gene is rarely studied in the environment. In this study, we examine the diversity of nirK in the marine pelagic environment, in light of previously described ecological patterns of pelagic thaumarchaeal populations. Phylogenetic analyses show that nirK better resolves diversification patterns of marine Thaumarchaeota, compared to the conventionally used marker gene amoA. Specifically, we demonstrate that the three major phylogenetic clusters of marine nirK correspond to the three ‘ecotype’ populations of pelagic Thaumarchaeota. In this context, we further examine the relative distributions of the three variant groups in metagenomes and metatranscriptomes representing two depth profiles in coastal Monterey Bay. Our results reveal that nirK effectively tracks the dynamics of thaumarchaeal ecotype populations, particularly finer‐scale diversification patterns within major lineages. We also find evidence for multiple copies of nirK per genome in a fraction of thaumarchaeal cells in the water column, which must be taken into account when using it as a molecular marker.

“…Data from various studies with model denitrifiers (Giannopoulos et al, ; Olaya‐Abril et al, ; Gaimster et al, ; Gaimster et al, ; Kohlmann et al, ; Thorgersen et al, ) and nitrifiers (Qin et al, ; Cho et al, ; Wei et al, ; Mellbye et al, ; Pérez et al, ; Lu et al, ; Carini et al, ) is available for integration into models. However, soil and aquatic environments host complex microbial communities that could differ substantially in terms of the regulation and activity with respect to their nitrogen‐cycling pathways (Lycus et al, ).…”

Section: Current and Future Methods For Assessing Sources And Sinks Omentioning

confidence: 99%

Systems biology approaches towards predictive microbial ecology

Otwell

Lomana

Gibbons

et al. 2018

Through complex interspecies interactions, microbial processes drive nutrient cycling and biogeochemistry. However, we still struggle to predict specifically which organisms, communities and biotic and abiotic processes are determining ecosystem function and how environmental changes will alter their roles and stability. While the tools to create such a predictive microbial ecology capability exist, cross-disciplinary integration of high-resolution field measurements, detailed laboratory studies and computation is essential. In this perspective, we emphasize the importance of pursuing a multiscale, systems approach to iteratively link ecological processes measured in the field to testable hypotheses that drive high-throughput laboratory experimentation. Mechanistic understanding of microbial processes gained in controlled lab systems will lead to the development of theory that can be tested back in the field. Using N O production as an example, we review the current status of field and laboratory research and layout a plausible path to the kind of integration that is needed to enable prediction of how N-cycling microbial communities will respond to environmental changes. We advocate for the development of realistic and predictive gene regulatory network models for environmental responses that extend from single-cell resolution to ecosystems, which is essential to understand how microbial communities involved in N O production and consumption will respond to future environmental conditions.