Marine microbes drive ocean biogeochemistry. The myriad of marine microbes are organized by which microbes respond to an environmental condition and which one are deterred or displaced by a set of environmental conditions. Environmental conditions such as presence or absence of light, concentration of limiting inorganic nutrients and the quantity and quality of bioavailable organic matter are examples of factors that can influence microbial community structure. My work used amplicon sequencing of the 16S rRNA gene a biological tracer to elucidate drivers of biogeochemical trends across coastal and open-ocean environments. In coral reefs, intense recycling of nutrients and organic matter supports highly productive coral reef systems despite being bathed in unproductive oligotrophic waters. Around the French Polynesian islands of Mo’orea and Tahiti, we combined 16S rRNA metabarcoding with a suite of biogeochemical measurements to resolve the origins and spatial influence of an Island Mass Effect, the observed enhancement in primary production surrounding coral reef atolls and islands. Additionally, within the Mo’orea coral reef system we characterized these unique reef microbial communities across a variety of physical regimes and reef habitats, linking bacterioplankton to gradients in biogeochemistry, physical wave forcing, and organic matter composition. Transitioning to open-ocean systems, we applied these methods at the Bermuda Atlantic Time-series site (BATS), one of the most well-studied sites in the global ocean. In open-ocean systems, particulate organic matter (POM) formed in the ocean’s surface plays a central role in the carbon cycle, with sinking POM acting as the dominant pathway in the biological carbon pump. We aimed to better resolve patterns of particle colonization and chemical transformation across depth and particle size, resolving drivers of organic particle attenuation and transformation as organic matter travels from the surface into the deep. Through this research, we utilize microbial community composition as a tracer to inform the origins of observed biogeochemical patterns and organic matter transformation in both coastal and open-ocean environments.

Phytoplankton blooms are major sources of net community production (NCP) in the Western North Atlantic and represent important sinks for atmospheric CO2, influencing the balance of carbon between the ocean and atmosphere. The organic matter produced by these blooms are subject to a variety of food web processes that dictate the partitioning of organic carbon into the particulate and dissolved phases. Some of the dissolved organic matter (DOM) is used to fuel instantaneous bacterial carbon demand (BCD) for biomass production and respiration. The DOM that resists or escapes rapid bacterioplankton utilization can accumulate, of which a fraction can persist. This persistent DOM is subject to being exported to depths below the sunlit ocean due to winter convective mixing and thus, can represent an important export pathway for carbon produced by phytoplankton blooms. This dissertation seeks to clarify the magnitude and divers of surface DOC accumulation over the course of the annual phytoplankton bloom in the Western North Atlantic, the contribution of DOC to annual vertical carbon export (aka biological carbon pump) via deep convective overturn, and the fate of surface accumulated DOC following physical export.

The concentration of atmospheric carbon dioxide (CO2) is increasing at extraordinary rates (e.g. Le Quéré et al. 2016). Effectively mitigating the impacts of increasing atmospheric CO2 on climate change, the ocean has absorbed roughly 30 % of the anthropogenic CO2 produced since the Industrial Revolution (e.g. Doney et al. 2009). However, increased levels of CO2 in the surface ocean may have lasting implications for marine biogeochemical cycles (e.g. Riebesell et al. 2013). In addition to gradual increases in concentrations of CO2 in the surface ocean through rising atmospheric CO2, mixing of deep water upwards leads to the injection of elevated partial pressures of CO2 (pCO2) into the surface ocean, exposing some areas of the surface ocean to transient pulses of elevated pCO2 equivalent to those projected for the year 2100 (Feely et al. 2008, Hofmann et al. 2011). This broad range of exposure to elevated pCO2, from ephemeral pulses to gradual increases, highlights the necessity to understand the impacts of pCO2 on marine biogeochemical processes on a variety of timescales.

Heterotrophic bacterioplankton play a key role in the biogeochemical cycling of carbon in the ocean through the consumption and remineralization of dissolved organic carbon (DOC). The physical mixing of DOC that accumulates in the surface ocean into the mesopelagic represents ~ 20 % of global annual organic carbon export (Hansell and Carlson 2015), making DOC export an important pathway in the biological carbon pump. Export of DOC to ocean depths removes this carbon from interaction with the atmosphere on a variety of timescales. Processes that remove or reduce the accumulation of DOC in the surface ocean can decrease the amount of DOC available for export and ultimately lessen the effectiveness of DOC export as a sink of carbon in the ocean. As the primary consumers of DOC, heterotrophic bacterioplankton can reduce the amount and rate of DOC accumulation in the surface ocean. Thus, factors that affect the ability of bacterioplankton to consume DOC can affect DOC accumulation and have implications for DOC export potential.

In Chapter I, I present results from seawater culture experiments that were designed to assess the effects of pCO2 on bacterioplankton consumption of DOC. Results from these experiments provide evidence that short-term exposure to elevated pCO2 can enhance the rate of removal of photosynthetically-derived surface DOC by natural bacterioplankton communities. To evaluate potential physiological and metabolic mechanisms responsible for these enhanced rates of DOC removal by marine bacterioplankton, I present results from a metagenomic analysis in Chapter II. These results suggest that elevated pCO2 can alter the taxonomic composition and metabolic potential of natural bacterioplankton communities. Collectively, Chapters I and II contribute to a growing understanding of the effects of elevated pCO2 on bacterioplankton-mediated carbon cycling in the surface ocean. Chapter III provides the first high-resolution evaluation of key physical and biogeochemical variables controlling carbon dynamics in the oligotrophic waters surrounding the islands of Moorea and Tahiti, French Polynesia, providing the context needed to predict how short-term increases in pCO2 may alter carbon-cycling in oligotrophic gyre ecosystems.

References

Doney, S.C., Fabry, V.J., Feely, R.A., and Kleypas, J.A. (2009). Ocean Acidification: The Other CO2 Problem. Annual Review of Marine Science 1, 169–192.

Feely, R.A., Doney, S.C., and Cooley, S.R. (2009). Ocean acidification: Present conditions and future changes in a high-CO₂ world. Oceanography 22, 36–47.

Hansell D.A. and Carlson, C.A. (2015). Biogeochemistry of marine dissolved organic matter (Amsterdam; Boston: Academic Press).

Hofmann, G.E., Smith, J.E., Johnson, K.S., Send, U., Levin, L.A., Micheli, F., Paytan, A., Price, N.N., Peterson, B., Takeshita, Y., et al. (2011). High-Frequency Dynamics of Ocean pH: A Multi-Ecosystem Comparison. PLoS ONE 6, e28983.

Le Quéré, C., Andrew, R.M., Canadell, J.G., Sitch, S., Korsbakken, J.I., Peters, G.P., Manning, A.C., Boden, T.A., Tans, P.P., Houghton, R.A., et al. (2016). Global Carbon Budget 2016. Earth System Science Data 8, 605–649.

Riebesell, U., Gattuso, J.-P., Thingstad, T.F., and Middelburg, J.J. (2013). Preface “Arctic ocean acidification: pelagic ecosystem and biogeochemical responses during a mesocosm study.” Biogeosciences 10, 5619–5626.

Approximately 50 percent of marine primary production passes through the dissolved organic matter (DOM) pool (Myklestad 2000; Nagata 2000). The major consumers of DOM are marine bacterioplankton, which can direct DOM down three pathways: respiration to inorganic constituents, incorporation into biomass, or modification or lack of consumption leading to persistence as DOM. The aspects of DOM source and composition that determine its bioavailability, and its interactions with the clades comprising the bacterial community, are broadly understood, but many of the finer details remain to be studied. This dissertation investigates bottom-up controls on bacterial community composition (BCC) and activity through a time-series study in the Santa Barbara Channel (SBC), CA, and examines the effects of phytoplankton DOM on bacterial metabolism, in field and laboratory experiments.

Chapter II describes the results of a four-year time-series study of BCC and metabolic activity in the SBC. BCC showed the greatest variability over depth; at the surface, the seasonal cycle was significantly more influential on BCC than spatial variability within cruises. Community types showed repeating patterns following the annual upwelling and phytoplankton bloom season; however, new community types appeared in the second half of the time-series, possibly in association with the Pacific warm anomaly observed in 2014. Individual operational taxonomic units (OTUs) were strongly correlated with environmental parameters, reflecting a successional pattern in OTUs following the spring upwelling. Seasonality was moderately repeatable in both the community as a whole and in individual OTUs, with long-term changes in BCC possibly linked to broader climatological phenomena.

In Chapter III, interactions between dissolved organic carbon (DOC) and bacterioplankton were examined during a diatom and Phaeocystis bloom in the SBC over 5 days following an upwelling event, encompassing phytoplankton physiological states from a healthy bloom through the onset of silicon (Si) stress. DOC bioavailability, bacterial growth, and BCC responses were assessed with dilution batch-culture bioassays. In these experiments, as the bloom state progressed: bacterioplankton DOC usage increased; bacterial growth efficiencies increased; and measureable DOC that accumulated during the bloom remained unutilized in the bioassays. Thus, DOC released by the plankton community during a bloom simultaneously contributes to several DOM pools of variable longevity.

In Chapter IV, the ecological role of carbon-rich DOM exuded by nutrient-stressed phytoplankton was assessed using DOM from four coastal diatoms following depletion of nitrogen (N), Si, or both N+Si. In bioassay experiments, short-term responses were affected both by diatom source species and by the nutrient stress under which the DOM was produced. Si-stress DOM was generally the most bioavailable over several days and led to higher bacterial growth efficiencies. However, the amount of diatom-derived DOC that persisted over months differed among source diatom species, with no evidence of a nutrient stress effect. The identity of the nutrient that terminates a phytoplankton bloom can therefore impact heterotrophic activity in the short term, while source phytoplankton species is more likely to influence DOC persistence in surface waters and its potential export.

There are more than 4000 lakes above 2500 m elevation in the Sierra Nevada of California. Recent developments in understanding of aquatic ecosystem function predict that metabolism and food web structure in these dilute, low-productivity lakes may be dominated by an active and diverse microbial community. The identity, activity, and importance of pelagic prokaryotic communities (bacterioplankton) in these ecosystems is little known, yet understanding the role of these organisms in lake metabolism and food web dynamics is critical to predicting the response of Sierra lakes to global change. This study combined range-wide surveys, multiannual seasonal monitoring, and experimental approaches to describe the biodiversity and biogeochemical role of bacterioplankton in high-elevation lakes of the Sierra Nevada. Particular attention was payed to determining the impacts of anthropogenic nutrient deposition and introduced salmonids on the structure and metabolism of microbial communities.

Our results indicate an abundant, remarkably diverse, and metabolically active bacterioplankton community. A three-year study of Emerald Lake, a representative cirque lake in Sequoia National Park, provided estimates of more than 250 bacterial phylotypes exhibiting predictable patterns of community phenology in response to seasonal transitions. Bacterial densities averaged 1 billion cells per liter throughout the year, and estimates of bacterioplankton biomass averaged 40% of total pelagic biomass. Rates of bacterial production were comparable to rates of net primary production, ranging from 1% during fall phytoplankton blooms to nearly 500% during snowmelt when terrestrial inputs of dissolved organic matter were highest. Bacterial metabolic properties were coupled to larger ecosystem dynamics, with growth efficiencies correlated with rates of primary productivity.

Phosphorus enrichment, but not nitrogen enrichment, produced rapid and sustained increases in bacterial production rates and produced significant alterations to bacterial community structure. The metabolic and community response to nutrient enrichment by the bacterioplankton was independent of phytoplankton responses, suggesting that microbial populations may be more sensitive indicators of eutrophication and ecosystem change. Among lakes throughout the Sierra Nevada, introduced salmonid fish had no significant relationship with multivariate bacterial community composition, but salmonid density did exhibit a significant positive correlation with bacterial phylotype richness and diversity, suggesting that trout introductions have altered bacterioplankton community structure. Within catchments bacterial communities exhibited decreasing similarity with increasing biogeographic distance, supporting the concept that macroecological principles of dispersal and isolation play a role in structuring communities of microorganisms.

This study highlights the importance of bacteria in lake ecosystems of the Sierra Nevada by providing spatially and temporally robust estimates of biomass, metabolism, diversity, and role in ecosystem biogeochemical processes. In addition to specifically defining impacts of introduced species and nutrient enrichment on microbial communities, it provides a sturdy ecological scaffolding for future studies of the role of microorganisms in high-elevation lake ecosystems.