Cryptic niche differentiation of novel sediment ecotypes of Ruegeria pomeroyi correlates with nitrate respiration

Abstract

Marine intertidal sediments fluctuate in redox conditions and nutrient availability, and they are also known as an important sink of nitrogen mainly through denitrification, yet how denitrifying bacteria adapt to this dynamic habitat remains largely untapped. Here, we investigated novel intertidal benthic ecotypes of the model pelagic marine bacterium Ruegeria pomeroyi DSS-3 with a population genomic approach. While differing by only 1.3% at the 16S rRNA gene level, members of the intertidal benthic ecotypes are complete denitrifiers whereas the pelagic ecotype representative (DSS-3) is a partial denitrifier lacking a nitrate reductase. The intertidal benthic ecotypes are further differentiated by using non-homologous nitrate reductases and a different set of genes that allow alleviating oxidative stress and acquiring organic substrates. In the presence of nitrate, the two ecotypes showed contrasting growth patterns under initial oxygen concentrations at 1 vol % versus 7 vol% and supplemented with different carbon sources abundant in intertidal sediments. Collectively, this combination of evidence indicates that there are cryptic niches in coastal intertidal sediments that support divergent evolution of denitrifying bacteria. This knowledge will in turn help understand how these benthic environments operate to effectively remove nitrogen.

Development and validation of an experimental life support system to study the impact of ultraviolet B radiation and temperature on coral reef microbial communities

“…In sediment, abundant OTUs were assigned to the genera Ruegeria (family Rhodeobacteraceae), Methyloceanibacter (family Methyloligellaceae) and Filomicrobium (family Hyphomicrobiaceae). Members of these families were previously found to be abundant in marine sediment and are known to play an important role in nutrient remineralization (Begmatov et al, 2021; Dong et al, 2022; Lin et al, 2022; Vekeman et al, 2016). Recently, Ruegeria strains isolated from marine sediment were observed to utilize various organic and inorganic compounds, oxidize sulfur, and perform complete denitrification by reducing nitrate to molecular nitrogen (Lin et al, 2022).…”

“…Members of these families were previously found to be abundant in marine sediment and are known to play an important role in nutrient remineralization (Begmatov et al, 2021; Dong et al, 2022; Lin et al, 2022; Vekeman et al, 2016). Recently, Ruegeria strains isolated from marine sediment were observed to utilize various organic and inorganic compounds, oxidize sulfur, and perform complete denitrification by reducing nitrate to molecular nitrogen (Lin et al, 2022). The Methyloligellaceae and Hyphomicrobiaceae families include bacterial species, which are able to reduce one-carbon compounds (methylotrophs) and oxidize methane under aerobic conditions (Vekeman et al, 2016).…”

Homogeneous environmental selection mainly determines the denitrifying bacterial community in intensive aquaculture water

“…Interestingly, Ruegeria was the dominant genus in the total, napA, and nosZ bacterial communities which is rarely reported and used in applications. Ruegeria is a common denitrifier carrying a complete gene set for denitrification in coastal environments (Lin et al, 2022;Meng et al, 2022). Therefore, future applications of denitrifying bacteria may target the isolation of the Ruegeria geneus.…”

“…We further found that Maribacter and Ruegeria were dominant taxa present in both the total bacterial community and the nosZ denitrifiers in the co-occurrence network (Supplementary Figure S13). This could be attributed to the high salinity tolerance and robust denitrification capabilities of Maribacter and Ruegeria in saline conditions (Li et al, 2013;Lin et al, 2022). Moreover, Maribacter is known to utilize lipid compounds, a primary ingredient in formulated feed, and its secondary metabolites may benefit denitrifers (Bonin et al, 2015).…”

Coastal Transient Niches Shape the Microdiversity Pattern of a Bacterioplankton Population with Reduced Genomes

“…For bacteria inhabiting marine environments, the use of this population genomics approach is in its infancy. It has been largely applied to lineages with large and variable genomes, such as the Vibrio ( 9 , 12 , 13 ) and Ruegeria lineages ( 14 – 16 ), that readily grow on solid media. In sunlit pelagic oceans, however, a typical bacterioplankton cell often carries a reduced genome (with an average genome size of 2.2 to 2.6 Mbp) ( 17 ).…”