Ecological Effects Of Rhodopsin Phototrophy In Antarctic Sea Ice

<p><strong>Despite its extreme cold temperatures and being in complete darkness for much of the year, Antarctic sea ice harbours a diverse and robust microbial community that is important for pelagic and benthic ecosystems in ice-dominated regions. Some of these bacteria employ rhodopsin-based phototrophy, a light-harvesting process that generates energy without fixing carbon, to survive in extreme conditions. First identified in 2000, the discovery of rhodopsin phototrophy disrupted the long-held view that most marine bacteria were obligate heterotrophs, and that 30-80% of the global marine bacterial community may exploit this hybrid photoheterotrophic pathway. Yet the ecosystem-level consequences of rhodopsin-driven energy flux, particularly in polar regions, remains poorly understood. This thesis investigates how rhodopsin-based photoheterotrophy and sea-ice variability influence microbial interactions, community composition, and broader ecological processes in the Southern Ocean.</strong></p><p>Chapter 1 introduces these knowledge gaps and presents background information necessary for understanding the research presented in this thesis. Antarctic sea ice serves as an ideal study system because its brine channels create a spatially and temporally stable gradient of irradiance, temperature, and salinity, within which rhodopsin expression could confer measurable ecological advantages. This chapter describes these physical aspects of sea ice, and reviews the sea-ice microbial community (SIMCO).</p><p>Chapter 2 presents a comparative framework for sea-ice ecosystem models, evaluating the Community Ice CodE (CICE), the Louvain-la-Neuve Sea-Ice Model in one dimension (LIM1D), a Nutrient-Phytoplankton-Zooplankton-Detritus (NPZD) model, and Qualitative Network Modelling (QNM). Each tool varies in computational complexity, physical-biological coupling, and data requirements. This assessment is an initial step and guide for choosing modelling framework that accurately capture microbial processes, including rhodopsin phototrophy, and their physical environment within Antarctic sea ice.</p><p>Chapter 3 uses QNM to investigate how rhodopsin-bearing (Rh+) and non-rhodopsin-bearing (Rh-) bacterial groups respond to changes in physical and ecological pressures. Press perturbations suggest that Rh+ bacteria capitalize on elevated light to outcompete Rh- bacteria, but viral outbreaks reduce overall system biomass. These findings suggest that rhodopsin-based phototrophy is a useful survival mechanism for a subset of sympagic bacteria, and that rhodopsin-driven energy-flux may be important in determining spatiotemporal patterns in bacterial community composition.</p><p>Chapter 4 tests the qualitative results of Chapter 3 with a field campaign in the Ross Sea during the spring-to-summer transition. 16s rRNA sequencing and epifluorescence microscopy were applied to samples taken across five depth horizons during the study period. Rh+ bacteria initially constituted nearly 15% of the bacterial community, during a time of the season with relatively cold temperatures and moderate light. Their peak relative abundance shifted from the ice-water interface to the mid- and upper-ice column as the season progressed. Together, these findings demonstrate that rhodopsin-based phototrophy provides a short-term survival advantage under physical extremes, but does not ensure widespread proliferation.</p><p>Chapter 5 links sea-ice microbial processes to the broader marine ecosystem through a case-study of Antarctic toothfish (Dissostichus mawsoni) recruitment. Generalized Additive Models and QNM results demonstrate that broad climatological processes associated with the Southern Oscillation Index control recruitment. However, older juveniles that likely become more motile and began active feeding, sea-ice microbial productivity, was a better predictor of the observed patterns in juvenile survival. Methodologically, a novel Cohort Survival Index was developed in an attempt to illuminate any detectable patterns associated within year-classes.</p><p>Chapter 6 synthesizes these findings, asserting that although rhodopsin-bearing bacteria are quantitatively modest in the sea-ice microbial community, rhodopsin phototrophy does represent a reliable survival mechanism in extreme polar conditions. This thesis integrated empirical research, statistical and qualitative modelling, to understand how rhodopsin-driven energy flux may modulate broader ecosystem processes. Thus, this research broadens our understanding of Antarctic marine and sea-ice ecology, and builds upon a growing body of foundational evidence for future research.</p>