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Journal Article
Tolar, BB, Ross MJ, Wallsgrove NJ, Liu Q, Aluwihare LI, Popp BN, Hollibaugh JT.  2016.  Contribution of ammonia oxidation to chemoautotrophy in Antarctic coastal waters. Isme Journal. 10:2605-2619.   10.1038/ismej.2016.61   AbstractWebsite

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 (mwean +/- 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 similar to 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 similar to 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 similar to 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.

Malfatti, F, Lee C, Tinta T, Pendergraft MA, Celussi M, Zhou YY, Sultana CM, Rotter A, Axson JL, Collins DB, Santander MV, Morales ALA, Aluwihare LI, Riemer N, Grassian VH, Azam F, Prather KA.  2019.  Detection of active microbial enzymes in nascent sea spray aerosol: Implications for atmospheric chemistry and climate. Environmental Science & Technology Letters. 6:171-177.   10.1021/acs.estlett.8b00699   AbstractWebsite

The oceans cover nearly three-quarters of the Earth's surface and produce vast quantities of sea spray aerosols (SSA). Studies have shown that due to ocean biology SSA particles are comprised of much more than just sea salt and often include proteins, lipids, sugars, viruses, and bacteria. In this study, we show for the first time that a diverse array of microbial enzymes (protease, lipases, and alkaline phosphatase) are transferred from the ocean into the atmosphere and often become even more active with measured activities in SSA particles that are 1-2 orders of magnitude higher than those in bulk seawater. We hypothesize that these enzymatic reactions are enhanced in the interfacial environment of droplets and aerosols that can dynamically modify surface chemical species and properties. Simulations reveal that enzyme-containing SSA particles can rapidly coagulate with other preexisting aerosols, thus transferring the impact of enzyme reactions to a broad range of marine aerosols. These biotic reaction pathways are expected to profoundly change the composition of marine aerosols, particularly at the interface, and thus will impact cloud properties in marine environments. Future studies are needed to determine how photochemistry, changing ocean conditions in a warming climate, and other external factors will influence the activities of these enzymes and their impact on the composition of the marine atmosphere.

Kharbush, JJ, Thompson LR, Haroon MF, Knight R, Aluwihare LI.  2018.  Hopanoid-producing bacteria in the Red Sea include the major marine nitrite oxidizers. Fems Microbiology Ecology. 94   10.1093/femsec/fiy063   AbstractWebsite

Hopanoids, including the extended side chain-containing bacteriohopanepolyols, are bacterial lipids found abundantly in the geological record and across Earth's surface environments. However, the physiological roles of this biomarker remain uncertain, limiting interpretation of their presence in current and past environments. Recent work investigating the diversity and distribution of hopanoid producers in the marine environment implicated low-oxygen regions as important loci of hopanoid production, and data from marine oxygen minimum zones suggested that the dominant hopanoid producers in these environments are nitrite-utilizing organisms, revealing a potential connection between hopanoid production and the marine nitrogen cycle. Here, we use metagenomic data from the Red Sea to investigate the ecology of hopanoid producers in an environmental setting that is biogeochemically distinct from those investigated previously. The distributions of hopanoid production and nitrite oxidation genes in the Red Sea are closely correlated, and the majority of hopanoid producers are taxonomically affiliated with the major marine nitrite oxidizers, Nitrospinae and Nitrospirae. These results suggest that the relationship between hopanoid production and nitrite oxidation is conserved across varying biogeochemical conditions in dark ocean microbial ecosystems.

Hansman, RL, Thurber AR, Levin LA, Aluwihare LI.  2017.  Methane fates in the benthos and water column at cold seep sites along the continental margin of Central and North America. Deep-Sea Research Part I-Oceanographic Research Papers. 120:122-131.   10.1016/j.dsr.2016.12.016   AbstractWebsite

The potential influence of methane seeps on carbon cycling is a key question for global assessments, but the study of carbon cycling in surface sediments and the water column of cold seep environments is complicated by the high temporal and spatial variability of fluid and gas fluxes at these sites. In this study we directly examined carbon sources supporting benthic and planktonic food webs at venting methane seeps using isotopic and molecular approaches that integrate this variability. At four seep environments located along North and Central America, microorganisms from two size fractions were collected over several days from 2800 to 90501 of seawater to provide a time-integrated measure of key microbial groups and the carbon sources supporting the overall planktonic microbial community. In addition to water column measurements, the extent of seafloor methane release was estimated at two of the sites by examining the stable carbon isotopic signature (delta C-13) of benthic metazoan infauna. This signature reveals carbon sources fueling the base of the food chain and thus provides a metric that represents a time-integrated view of the dominant microbial processes within the sediment. The stable carbon isotopic composition of microbial DNA (delta C-13-DNA), which had values between -17.0 and -19.5%(0), indicated that bulk planktonic microbial production was not ultimately linked to methane or other C-13-depleted seep-derived carbon sources. Instead these data support the importance of organic carbon derived from either photo- or chemoautotrophic CO2 fixation to the planktonic food web. Results of qPCR of microbial DNA sequences coding for a subunit of the particulate methane monooxygenase gene (pmoA) showed that only a small percentage of the planktonic microbial community were potential methane oxidizers possessing pmoA (< 5% of 16S rRNA gene copies). There was an overall decrease of C-13-depleted carbon fueling the benthic metazoan community from 3 to 5 cm below the seafloor to the sediment surface, reflecting limited use of isotopically depleted carbon at the sediment surface. Rare methane emission as indicated by limited aerobic methane oxidation acts to corroborate our findings for the planktonic microbial community.

Samo, TJ, Pedler BE, Ball GI, Pasulka AL, Taylor AG, Aluwihare LI, Azam F, Goericke R, Landry MR.  2012.  Microbial distribution and activity across a water mass frontal zone in the California Current Ecosystem. Journal of Plankton Research. 34:802-814.   10.1093/plankt/fbs048   AbstractWebsite

Ocean fronts with accumulated biomass and organic matter may be significant sites of enhanced microbial activity. We sampled a frontal region (the A-Front) separating oligotrophic and mesotrophic water masses within the California Current Ecosystem (CCE) to assess the influence of frontal hydrography on several microbial parameters. Samples for heterotrophic bacterial, viral and flagellate abundance, dissolved and particulate carbon and nitrogen, transparent particles and bacterial carbon production were collected at 6 depths from the surface to 100 m with 59 conductivity/temperature/depth casts along a 26-km northerly transect across the front. Relative to adjacent oligotrophic and mesotrophic waters, the frontal transition displayed peaks in the mean estimates of cell-specific bacterial carbon and bulk bacterial production, particulate organic carbon and particulate organic nitrogen concentrations, and the abundance and size of transparent particles. Bacterial carbon production increased approximate to 5-fold northward from oligotrophic waters to the frontal zone, in agreement with an increase in the frequency of dividing cells, but bacterial abundance was lower than at adjacent stations. This may be partially explained by high chlorophyll, elevated virus:bacteria ratios and low nanoflagellate grazer abundance at the front. Our data suggest that CCE fronts can facilitate intense biological transformation and physical transport of organic matter, in sharp contrast to adjacent low productivity waters, and harbor dynamic microbial populations that influence nutrient cycling.