Dynamics of Thaumarchaeota Populations in Southeastern USA Coastal Waters
James T. Hollibaugh1*, Annie Bratcher1, Jelani B. Cheek1, Qian Liu1,2, Erica Malágon1, Brian N. Popp3,Meredith J. Ross1, Sylvia C. Schaefer1, Corinne M. Sweeney1, Bradley B. Tolar1,4, Constant M. G. van den Berg5,Natalie J. Wallsgrove3and Hannah Whitby5,6
1) Department of Marine Sciences, University of Georgia, Athens GA 30602-3636
2) Present address: Second Institute of Oceanography, Hangzhou, Zhejiang, China 310012
3) Department of Geology and Geophysics, University of Hawai‘i, Honolulu, HI 96822
4) Present address: Dept. of Earth System Science, Stanford University, Stanford, CA 94305
5) University of Liverpool, Liverpool, L69 3GP UK
6) Present address:LEMAR, Technopole Brest Iroise, Plouzané, F29280 France
*) Corresponding author: ; (v) 706/542-7671; (f) 706/542-5888
ABSTRACT
Sampling over a period of 8 yearsat Marsh Landing, Sapelo Island, Georgia, USA has revealedconsistent, mid-summer peaks in the abundance of Thaumarchaeota (“blooms,” 100-1,000-fold increases in abundance) accompanied by spikes in nitrite concentration. Hypotheses to explain the bloom include: advection or mixing from population centers adjacent to the study site; resuspension via bioturbation of populations living in sediments; and in situ growth controlled by seasonally varying environmental conditions. We collected data on rates of ammonia oxidation and the distribution of Thaumarchaeota and environmental variables during 6 transects of the South Atlantic Bight (SAB)in 2014 to evaluate the areal extent and timing of the bloom. We collected data on populations of Thaumarchaeota in surficial sediments adjacent to the study site over the same time period to test the bioturbation hypothesis.
The abundance of Thaumarchaeota 16S rRNA (rrs) and amoAgenes increased at inshore and nearshore stations beginning in July and peaked in mid-August at >107 copies L-1, as seen previously at Marsh Landing. The bloom did not extend onto the mid-shelf, where the abundance of Thaumarchaeota genes ranged from 103 to 105 copies L-1 year-round. Thaumarchaeota were also abundant in oxygen-deficient,subsurface waters at the shelf-break; however, this population did not display the same seasonality as,and was phylogenetically distinct from, the inshore population. Ammonia oxidation rates were highest (850 nmol L-1 d-1) at inshore stations and were at the limit of detection at mid-shelf stations. Seasonality of Thaumarchaeota populations in surficial sediments differed from the water column (lower abundance in mid-summer), and they were phylogenetically distinct. Thaumarchaeota populations in surficial sediment may have been reduced by high temperatures (>45 oC) from solar heating when sediments were exposed during mid-summer low tides.
Analysis of environmental data suggests that the seasonal distribution of Thaumarchaeota and ammonia oxidation rates in the SAB is controlled primarily by water temperature. The spatial distributions of Thaumarchaeota genes and ammonia oxidation rates during the bloomwere correlated with PAR attenuation coefficients and OBS measurements (Spearman’s R = 0.74and 0.67 for rrs vs PAR attenuation and OBS, respectively), suggesting that increasing water clarity along the onshore to offshore transect limited the development of Thaumarchaeota populations offshore. Experiments with enrichment cultures indicatethat nitrite accumulates in response to uncoupling of ammonia- and nitrite-oxidation at temperatures between 20 and 30 oC; temperatures >40oC are lethal to AOA. The bloom occurred despite concentrations of Cu2+(0.9-7.5 fM) that are significantly lower than those thought to limit growth (pM), suggesting that this population is able to access Cu from a dissolved pool (~10 nM) that is strongly bound by ligands (thiols and humic substances).
Clonedamplicons generated from DNA collected at mid-shelf stations using Archaea rrs primers were dominated by Marine Group II Archaea, whereas libraries from inshore and nearshore stations were dominated by members of the Nitrosopumilaceae closely related to several isolates, including the type strain. The population from the shelf-break ODZ was more diverse than the inshore population and was most similar to environmental sequences and SAGs from the deep ocean.