Orellana, Luis H

Abstract The majority of marine nitrite-oxidising bacteria (NOB) belong to three uncultured genera within the Nitrospinaceae family and thus the ecophysiology of these main nitrate producing microorganisms in the ocean remains poorly resolved. Here, we report on the environmental characterization of one of these genera, which we name Candidatus Nitromaricola. A single species within this genus, Candidatus Nitromaricola pontica, comprises >95% of the nitrite-oxidising community in the permanently stratified Black Sea. This provided a unique opportunity to study this globally abundant genus in situ, across pronounced environmental gradients of oxygen and inorganic nitrogen concentrations. We show that Ca. Nitromaricola pontica is capable of oxidising nitrite at similar rates in both oxic and apparently anoxic waters, although it had a higher abundance in the more oxygenated waters of the Black Sea. The genome of Ca. Nitromaricola pontica indicates that like other NOB, it is a chemolithoautotroph, oxidising nitrite, and fixing inorganic carbon. However, Ca. Nitromaricola pontica and other members of the Ca. Nitromaricola genus lack canonical high affinity terminal oxidases found in some other NOB genera. Single-cell analyses confirmed active autotrophic growth and showed that ammonium and urea, rather than nitrite, were the main nitrogen sources for biomass production. Our findings identify Ca. Nitromaricola as a globally abundant marine NOB and highlight its cosmopolitan lifestyle.

Abstract Marine algae annually sequester petagrams of carbon dioxide into polysaccharides, which are a central metabolic fuel for marine carbon cycling. Diatom microalgae produce sulfated polysaccharides containing methyl pentoses that are challenging to degrade for bacteria compared to other monomers, implicating these sugars as a potential carbon sink. Free-living bacteria occurring in phytoplankton blooms that specialise on consuming microalgal sugars, containing fucose and rhamnose remain unknown. Here, genomic and proteomic data indicate that small, coccoid, free-living Verrucomicrobiota specialise in fucose and rhamnose consumption during spring algal blooms in the North Sea. Verrucomicrobiota cell abundance was coupled with the algae bloom onset and accounted for up to 8% of the bacterioplankton. Glycoside hydrolases, sulfatases, and bacterial microcompartments, critical proteins for the consumption of fucosylated and sulfated polysaccharides, were actively expressed during consecutive spring bloom events. These specialised pathways were assigned to novel and discrete candidate species of the Akkermansiaceae and Puniceicoccaceae families, which we here describe as Candidatus Mariakkermansia forsetii and Candidatus Fucivorax forsetii. Moreover, our results suggest specialised metabolic pathways could determine the fate of complex polysaccharides consumed during algae blooms. Thus the sequestration of phytoplankton organic matter via methyl pentose sugars likely depend on the activity of specialised Verrucomicrobiota populations.