Abstract
Host-associated microbial communities have a strong influence on host health and biology and are therefore of increasing research interest. Within marine ecosystems, macroalgal microbiomes are major contributors to host development and morphology. Such systems are subject to increasing frequency of disturbances and extreme events resulting from anthropogenic global warming, which is also expected to lead to widespread range shifts. Understanding microbiome structure and assembly processes throughout a host species’ dispersal and establishment stages is therefore critical to enable us to predict species’ responses to climate change, and to inform management action. However, movement scenarios are particularly hard to study within natural ecosystems as a result of the rarity of dispersal events, as well as variability in environmental conditions and host habitat preferences.
Using a combination of ecological theory, 16S amplicon data, host genomics, and oceanographic techniques, I explore how the microbiomes of Durvillaea are structured across dispersing hosts, newly established populations, and older (‘stable’) populations. I start by building a theoretical framework to understand how microbial communities might respond to dispersal / movement processes. Principally, I suggest that dispersing microbial communities are most shaped by interactions between dispersal frequency (regular vs irregular, for example migration vs chance long distance-dispersal), community type (internal or external), and changes in selective processes or strength (e.g., community scale adaptation, or host decomposition).
To test the theoretical framework, I subsequently leverage Durvillaea’s high dispersal capacity to examine, using empirical data, dispersal-associated microbiome shifts relative to healthy attached populations. Examining the microbiomes of kelp rafts found off the coast of Otago, I found that dispersal leads to profound changes in the community – the core microbes found on attached kelp give way to a few abundant taxa, and many rare taxa, in rafts. Additionally, changes in both microbial species richness and composition are strongly linked to variability in sea surface temperature rather than length of time a raft spent at sea. These changes are associated with increased contributions of neutral processes shaping community assembly, resulting in increased dispersal limitation of microbiomes, and higher abundance of disease associated microbes.
Using an opportunity created by a localized population extirpation following a major (7.8 magnitude) earthquake in New Zealand in 2016, which led to widespread coastal uplift of up to ~6m, I test hypotheses relating to how population density affects microbiomes. I found that newly established, recovering, low density populations had higher functional, taxonomic, and phylogenetic beta-diversity than high density populations with regards to taxonomic variability. My analyses suggest that these changes are driven by dispersal limitation being stronger in low density populations than in established, high-density populations.
I explore the biogeographic relationship between microbiome composition and the genetic, environmental, and geographic structure of the host populations. I show that although host and microbiome exhibit shared biogeographic structure, these arise from different processes – with host biogeography showing classic signs of geographic distance decay, but the microbiome showing environmental distance decay. I show that as microbes become less common, the dominant ecological processes shift away from selective processes and towards neutral processes such as ecological drift, which is associated with reduced geographic structure in the microbiome. My findings suggest that the Baas Becking hypothesis of “everything is everywhere, the environment selects” may be a useful hypothesis to understand biogeography of macroalgal microbiomes.
To facilitate genomic analyses of the host, I used a joint nanopore and Illumina sequencing approach to sequence and assemble the genome of D. antarctica. Large amounts of genetic data exist for this species, but comprehensive analyses of these data are limited by the lack of an available genome assembly. This genome consists of 711 scaffolds, with an N50 of 773 kbp, and 15,084 annotated genes, and is of greater or comparable quality to other available brown algal genomes.