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

Environ Microbiol. 2019 Nov;21(11):4032-4045. doi: 10.1111/1462-2920.14753. Epub 2019 Aug 9.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Ammonia / metabolism
  • Archaea / classification*
  • Archaea / genetics*
  • Archaea / metabolism
  • Bays / microbiology*
  • Ecotype
  • Energy Metabolism / genetics*
  • Genetic Markers / genetics
  • Genetic Variation / genetics
  • Nitrite Reductases / genetics*
  • Nitrite Reductases / metabolism
  • Oxidation-Reduction
  • Phylogeny

Substances

  • Genetic Markers
  • Ammonia
  • Nitrite Reductases
  • nitrite reductase, copper-containing