Localized high abundance of Marine Group II archaea in the subtropical Pearl River Estuary: implications for their niche adaptation

Abstract

Marine Group II archaea are widely distributed in global oceans and dominate the total archaeal community within the upper euphotic zone of temperate waters. However, factors controlling the distribution of MGII are poorly delineated and the physiology and ecological functions of these still-uncultured organisms remain elusive. In this study, we investigated the planktonic MGII associated with particles and in free-living forms in the Pearl River Estuary (PRE) over a 10-month period. We detected high abundance of particle-associated MGII in PRE (up to ∼10 16S rRNA gene copies/l), which was around 10-fold higher than the free-living MGII in the same region, and an order of magnitude higher than previously reported in other marine environments. 10‰ salinity appeared to be a threshold value for these MGII because MGII abundance decreased sharply below it. Above 10‰ salinity, the abundance of MGII on the particles was positively correlated with phototrophs and MGII in the surface water was negatively correlated with irradiance. However, the abundances of those free-living MGII showed positive correlations with salinity and temperature, suggesting the different physiological characteristics between particle-attached and free-living MGIIs. A nearly completely assembled metagenome, MGIIa_P, was recovered using metagenome binning methods. Compared with the other two MGII genomes from surface ocean, MGIIa_P contained higher proportions of glycoside hydrolases, indicating the ability of MGIIa_P to hydrolyse glycosidic bonds in complex sugars in PRE. MGIIa_P is the first assembled MGII metagenome containing a catalase gene, which might be involved in scavenging reactive oxygen species generated by the abundant phototrophs in the eutrophic PRE. Our study presented the widespread and high abundance of MGII in the water columns of PRE, and characterized the determinant abiotic factors affecting their distribution. Their association with heterotrophs, preference for particles and resourceful metabolic traits indicate MGII might play a significant role in metabolising organic matters in the PRE and other temperate estuarine systems.

Genomic ecology of Marine Group II, the most common marine planktonic Archaea across the surface ocean

“…Cluster 3, which was relatively more abundant in the surface and DCM, co-occurred with a catalase gene previously seen on MGII contigs (Tully, Sachdeva, Graham, & Heidelberg, 2017;Xie et al, 2018). The presence of a catalase gene suggests that some MGII have to deal with oxidative stress associated with phototrophs that produce reactive oxygen species (Xie et al, 2018).…”

“…Another study separated five different subclades of MGII proteorhodopsin (Tully, 2019) following nomenclature from (Boeuf, Audic, Brillet-Guéguen, Caron, & Jeanthon, 2015;Pinhassi, DeLong, Béjà, González, & Pedrós-Alió, 2016). Other metagenomics fragments suggest that some MGIIa could live associated to particles, and that they could be motile and degrade polymers like proteins and lipids (Iverson et al, 2012;Rinke et al, 2018;Tully, 2019;Xie et al, 2018). Recently, Xie et al (2018) presented a new partially reconstructed MGIIa genome, the MGIIa_P, which contained higher proportions of glycoside hydrolases indicative of the ability to hydrolyse glycosidic bonds.…”

Impacts of Salinity and Oxygen on Particle-Associated Microbial Communities in the Broadkill River, Lewes DE

“…Additionally, the Thermoplasmata, while present at abundances >1% in all size fractions and across the entire salinity gradient, was overwhelmingly dominant in the marine station on both particle sizes. The Thermoplasmata present in this station were mostly composed of Group II Euryarchaeota, an archaeal group that has been well documented in coastal marine waters (DeLong, 1992;Galand et al, 2008;Xie et al, 2018). A recent study from the Pearl River Estuary found that Group II Euryarchaeota are dominant in marine water, but not as common in brackish water (Xie et al, 2018).…”

“…The Thermoplasmata present in this station were mostly composed of Group II Euryarchaeota, an archaeal group that has been well documented in coastal marine waters (DeLong, 1992;Galand et al, 2008;Xie et al, 2018). A recent study from the Pearl River Estuary found that Group II Euryarchaeota are dominant in marine water, but not as common in brackish water (Xie et al, 2018). The increased relative abundance of the Halobacteria downstream and the dominance of Thermoplasmata in the marine station is likely related to increasing salinity, showing that in addition to anaerobic stress, salinity is an important factor in determining archaeal community composition.…”

Transcriptional activity differentiates families of Marine Group IIEuryarchaeotain the coastal ocean

“…Poseidoniales abundance is 10 6 -10 7 genes or cells L -1 in oligotrophic waters [62][63][64][65][66] and 10 7 -10 8 genes or cells L -1 in coastal waters [9,54,56,[67][68][69]. Greater gene abundance in inshore, nearshore, and mid-shelf waters indicates Ca.…”