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Link to original content: https://pubmed.ncbi.nlm.nih.gov/27187795/
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. 2016 Nov;10(11):2605-2619.
doi: 10.1038/ismej.2016.61. Epub 2016 May 17.

Contribution of ammonia oxidation to chemoautotrophy in Antarctic coastal waters

Bradley B Tolar  1   2 , Meredith J Ross  1 , Natalie J Wallsgrove  3 , Qian Liu  1 , Lihini I Aluwihare  4 , Brian N Popp  3 , James T Hollibaugh  1
Affiliations

Contribution of ammonia oxidation to chemoautotrophy in Antarctic coastal waters

Bradley B Tolar et al. ISME J. 2016 Nov.

Abstract

There are few measurements of nitrification in polar regions, yet geochemical evidence suggests that it is significant, and chemoautotrophy supported by nitrification has been suggested as an important contribution to prokaryotic production during the polar winter. This study reports seasonal ammonia oxidation (AO) rates, gene and transcript abundance in continental shelf waters west of the Antarctic Peninsula, where Thaumarchaeota strongly dominate populations of ammonia-oxidizing organisms. Higher AO rates were observed in the late winter surface mixed layer compared with the same water mass sampled during summer (mean±s.e.: 62±16 versus 13±2.8 nm per day, t-test P<0.0005). AO rates in the circumpolar deep water did not differ between seasons (21±5.7 versus 24±6.6 nm per day; P=0.83), despite 5- to 20-fold greater Thaumarchaeota abundance during summer. AO rates correlated with concentrations of Archaea ammonia monooxygenase (amoA) genes during summer, but not with concentrations of Archaea amoA transcripts, or with ratios of Archaea amoA transcripts per gene, or with concentrations of Betaproteobacterial amoA genes or transcripts. The AO rates we report (<0.1-220 nm per day) are ~10-fold greater than reported previously for Antarctic waters and suggest that inclusion of Antarctic coastal waters in global estimates of oceanic nitrification could increase global rate estimates by ~9%. Chemoautotrophic carbon fixation supported by AO was 3-6% of annualized phytoplankton primary production and production of Thaumarchaeota biomass supported by AO could account for ~9% of the bacterioplankton production measured in winter. Growth rates of thaumarchaeote populations inferred from AO rates averaged 0.3 per day and ranged from 0.01 to 2.1 per day.

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Figures

Figure 1
Figure 1
Abundance of Thaumarchaeota amoA versus rrs genes in samples from Antarctic continental shelf waters. Symbols represent water masses and dates sampled as shown in the legend. Late winter samples (filled symbols) were collected in September 2010. Summer samples (open symbols) were collected in January 2011. Upper Antarctic surface water (UAASW, filled circles); lower AASW (LAASW, filled squares); and CDW (filled triangles); WW (squares); and CDW (triangles). A line of slope=1 is shown for reference.
Figure 2
Figure 2
Abundance of Thaumarchaeota ureC genes in samples from Antarctic continental shelf waters compared with the abundance of (a) archaeal amoA and (b) Thaumarchaeota rrs genes in the same sample. Symbols represent water masses and dates sampled as in Figure 1. Lines of slope=1 are shown for reference.
Figure 3
Figure 3
Abundance of Archaea amoA genes versus Archaea amoA transcripts in samples from Antarctic coastal waters. Symbols represent water masses and dates sampled as in Figure 1. A line of slope=1 is shown for reference.
Figure 4
Figure 4
Relationship between AO rate and gene and transcript abundance. Panels show AO rates plotted against: (a) archaeal rrs gene abundance; (b) archaeal amoA gene abundance; (c) archaeal amoA transcript abundance; and (d) the ratio of archaeal amoA transcripts to genes (mRNA/DNA). Symbols represent water masses and dates sampled as in Figure 1.
Figure 5
Figure 5
Phylogenetic analysis of Archaea amoA sequences retrieved from the study area. Partial sequences (359 bp) of Thaumarchaeota amoA genes obtained by high-throughput sequencing were aligned against the Pester et al. (2012) database and the neighbor-joining tree was constructed in ARB. OTUs were defined at 97% similarity. Numbers following each OTU give the number of sequences and % of total sequences it represents. Additional notations apply to four major clades to indicate the % of sequences in these clades from each water mass sampled (AASW—green; WW—blue; CDW—red). Shading of trapezoids representing sequences assigned to four major clades indicates the relative contribution of sequences from AASW+WW (blue) versus all CDW (red) to these clades. Dashed boxes delineate archaeal amoA groups A (surface water) and B (deep water) as defined in Francis et al. (2005). Only bootstrap values ⩾50% (of 1000 iterations) are shown.
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