Laura Parfrey

There is a growing recognition of the important role that host-associated microbes play in the biology and health of seaweeds. The seaweed cultivation industry is rapidly expanding due to its high demand for various applications and as a nutritious food source. As a result, there is a growing interest in exploring the potential for manipulating the microbiome to improve seaweed aquaculture and identify potential probiotic strains more effectively. Recent studies have highlighted an increase in disease and a decline in crop yields in seaweed aquaculture, which can be attributed to intensified and global distribution. However, our current understanding of the influence of microbes on seaweed cultivation remains limited. The distribution of bacteria within the microbiome of seaweeds naturally varies both in space and time. The core microbiome hypothesis suggests that bacteria consistently present in the microbiome of hosts are more likely to play an important functional role. This makes the core bacteria an appealing target for microbial manipulation. In my research, I aim to test the core microbiome hypothesis, which suggests that the ecological distribution of bacteria can serve as a predictive factor for their influence on host biology. In Chapter 2, I developed a better understanding of the distribution of seaweed-associated bacteria and show how different ways of defining the core microbiome result in different suites of bacteria identified as the core, and conclude that sampling across broader spatial and temporal scales result in a more robust set of core bacteria. I found that most of these core bacteria from Fucus distichus were also widespread across seaweed species. In Chapter 3, I identified core bacteria associated with wild sugar kelp (Saccharina latissima) and their distribution on cultivated S. latissima. I then conducted experimental tests investigating the impact of microbial manipulation on S. latissima biology using bacterial isolates in the cultivation of S. latissima. The results revealed that bacteria can indeed alter growth and development of sugar kelp, and found a positive correlation between bacterial taxa found at high frequency on wild S. latissima and their effect on S. latissima development. Chapter 4 tested the prediction that the bacteria most commonly found on wild kelp (the core) would be more successful at colonizing kelp in laboratory cultures. Overall, my findings suggest that selecting probiotic strains from the core candidates could be a valuable strategy, as they are more likely to influence host biology and colonize kelp in a deterministic manner.

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Eelgrass (Zostera marina) is a coastal marine angiosperm found in the Northern Hemisphere and forms expansive meadows in sheltered estuaries and bays, providing habitat for a high diversity of organisms, including algae, invertebrates, microbes, fish, birds, and mammals. It also provides invaluable ecosystem services for humans, including coastal storm protection, carbon sequestration, and nutrient cycling. However, eelgrass meadows are threatened worldwide by numerous anthropogenic activities, including shoreline modification, overfishing, land-based nutrient loading, and climate change. In British Columbia, Canada, eelgrass ecosystems are vulnerable to human activities such as habitat destruction, fishing, and pollution, and warming waters, which can cumulatively lead to negative impacts on eelgrass and associated fauna. To understand how environmental variation and BC-specific human activities affect eelgrass ecosystems temporally and spatially, I used a three-year, monthly observational time series of two trophic groups, statistical modeling, and an experiment to study how eelgrass communities and species interactions vary at the micro and macro scales. I show that eelgrass and epiphytic algae biomass change seasonally, and the timing of their peak biomasses varies interannually and is driven by nutrient availability and mesograzer abundances. I also show that human activities have a negative effect on eelgrass biomass, epiphytic algae, and epifaunal invertebrate abundances and species richness. Lastly, I show the first experimental evidence that eelgrass leaves host a core microbiota, eelgrass leaf-associated microbial communities are primarily driven by their surrounding environment, yet there may be host influence because microbial communities are resistant to environmental change within short periods of time. This research provides new insight to how environmental variability and human activities shape eelgrass-associated epifauna communities. This information can be used to predict how eelgrass ecosystems may change over time, which can help inform management decisions for restoration and conservation practices. Implementing more regulations for coastal anthropogenic activities may help ensure that eelgrass, and the organisms and humans that depend on it, will be sustained well into the future.

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The microbiome of marine organisms contributes to host health and ecosystem processes like nutrient cycling. Despite the importance to healthy ecosystems, little is known about the dynamics and drivers of microbiome variation on marine hosts. In this dissertation, I use longitudinal studies and field-based transplant experiments to assess the factors associated with microbiome change on four coastal foundation species. In the intertidal macroalga Fucus distichus, I characterize temporal dynamics and microbiome variation on host individuals. I show seasonal turnover is a highly significant predictor of microbiome change. Local environmental conditions and host developmental stage also explain some microbiome variation. I test microbiome fidelity to geographically and phenotypically differentiated F. distichus by exposing hosts to new abiotic conditions and microbial source pools. No immediate shifts in microbiome composition occur in five-day transplant experiments, suggesting the established microbiome is buffered against short-term environmental change. I test whether host filtering modulates the shell microbiome of the mussel, Mytilus californianus, and find the microbiome is not specific to living mussels. Instead, it is associated with abiotic conditions that vary across geographic locations and elevation in the intertidal zone. In cultivated kelps, I test if outplanting kelp from controlled hatcheries to open ocean sites alters the microbiome and if host and abiotic factors are correlated with microbiome variation at cultivation sites. Host-species specificity was evident throughout the cultivation process and outplanting is followed by high microbiome turnover. Microbiome variation is more strongly correlated to season than abiotic differences between cultivation sites. Altogether, my findings suggest abiotic factors and host identity influence selective microbiome assembly on coastal foundation species. Seasonal microbiome turnover occurs in multiple hosts and coastal habitats, indicating microbes associated with the prevailing conditions may commonly replace existing members of the microbiome over weeks to months. Within host species, local abiotic conditions and host physiological state are correlated to microbiome variation. This research broadens our understanding of the tempo of microbiome turnover and factors predicting microbial community variation in marine foundation species. It provides necessary foundational knowledge for a holistic understanding of host and ecosystem response to changing oceans.

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Animals live with a symbiotic community of bacteria, and some of these bacteria affect host biology. Generally, these bacterial communities are diverse and complex. A key question in microbiome research is whether bacteria are specific to a host and affect host biology. In my dissertation, I use observational and experimental approaches to 1) understand the factors that contribute to composition of host-microbiota, 2) determine the core bacteria of a host by comparing the abundance of host bacteria to the bacteria in environmental bacterial communities, 3) determine the phylogenetic and environmental distribution of core bacteria and their close relatives to better understand their natural history, and 4) test whether core bacteria are correlated with aspects of host biology. Across three host species, I found bacterial communities that were populated by a few common and prevalent core bacteria that are absent from the environment; in most cases, these core bacteria belong to host-associated clades of bacteria. In chapter 2, I characterize the microbiota of the keystone sea star Pisaster ochraceus, identify core bacteria, and use phylogenetic trees to assess the distribution of their relatives. In chapter 3, I study the interactions between the skin microbiota and host innate immunity of Columbia spotted frogs and to determine whether they explain the occurrence of the amphibian pathogen, Batrachochytrium dendrobatidis (Bd). In chapter 4, I characterize the microbiota of wild and captive endangered Oregon spotted frogs (OSF) and whether their skin bacteria are associated with Bd intensity. Lastly, I experimentally test the hypothesis environmental reservoirs of bacteria influence the bacteria on the skins of frogs. Understanding the factors that structure captive communities has substantial conservation implications for captive breeding and head start programs. My results differ from previous studies by comparing the host to their environment and focusing on specific core bacteria.

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