Marine microbial community dynamics and responses to ocean acidification

Abstract

Marine microbes, including both eukaryotes and prokaryotes, are the basal components of marine food webs and play a fundamental role in global biogeochemical cycling. Marine phytoplankton are responsible for approximately 50% of Earth’s primary production, while heterotrophic bacteria and archaea modulate carbon and nutrient cycling in the marine environment. The structure and function of marine microbial communities are closely coupled. Consequently, understanding the factors which govern the distribution of marine microbes through space and time has key implications for food webs and biogeochemical cycling. The development of high-throughput sequencing technologies has revolutionised marine microbial ecology by facilitating the profiling of microbial communities in high taxonomic resolution. In this thesis high-throughput sequencing of the 16S and 18S rRNA genes was used to achieve two major aims. The first aim was to investigate the ecological processes which underpin microbial community assembly in the marine environment. The second aim was to investigate the responses of marine microbial communities to near- future ocean acidification. Two studies were performed towards the first aim of this thesis. In the first study, the microbial biogeography of the South Pacific Gyre was characterised across three depths at 22 stations along a 2,000 km longitudinal transect of the region. Microbial community composition was homogenous across horizontal spatial scales in the surface waters of the South Pacific Gyre, but varied significantly between surface waters and the deep chlorophyll maximum. A null model approach was used to unveil the ecological processes driving microbial community assembly in the region. Microbial communities in the surface waters were assembled primarily through the deterministic process of homogeneous selection, indicating that selection pressures were sufficient to overwhelm the influence of dispersal effects and ecological drift across vast horizontal spatial distances in the region. Dispersal limitation was comparatively more influential in the assembly of microbial communities between the surface waters and the deep chlorophyll maximum, indicating that stochastic processes play a significant role in microbial community assembly between these contiguous water masses. In the second study, the bacterioplankton and protist biogeography of the Southland Front system was characterised in surface waters at 24 stations spanning four water masses. Both bacterioplankton and protist communities displayed significant structuring according to water mass, although this effect was most pronounced in bacterioplankton communities. A null model approach revealed that bacterioplankton communities were primarily assembled through homogeneous selection, while protist communities were primarily assembled through dispersal limitation and ecological drift across the Southland Front system. These findings highlight that distinct ecological processes can underpin the assembly of co- occurring bacterioplankton and protist communities, and that hydrographic features such as oceanic fronts play an important role in structuring both bacterioplankton and protist communities. Two studies were conducted towards the second aim of this thesis. In the first study, the effect of ocean acidification and warming on bacterioplankton communities was investigated at the fringe and ultra-oligotrophic centre of the South Pacific Gyre using trace-metal clean deckboard incubation experiments. Bacterioplankton community composition and function were resistant to ocean acidification alone, and combined with warming, at the fringe of the South Pacific Gyre. Subtle but significant responses of bacterioplankton community composition to ocean acidification were observed at the ultra- oligotrophic centre of the South Pacific Gyre. These results suggest that bacterioplankton community responses to ocean acidification may be modulated by nutrient regimes. Nonetheless, the findings of this study did not diverge substantially from the narrative that bacterioplankton communities are resistant to near-future acidification. In the second study, the effect of ocean acidification on both prokaryotic and eukaryotic biofilm communities was investigated at the Shikine-Jima CO2 seep system in Japan. The composition of both prokaryotic and eukaryotic communities was profoundly affected by ocean acidification through early successional stages, though these responses were not associated with shifts in community diversity or evenness. Notably, the relative abundance of the nuisance algae Prymnesium sp. and Biddulphia biddulphiana were enhanced under high CO2 conditions. These findings suggest that benthic biofilm communities may be vulnerable to near-future ocean acidification, and that changes in biofilm community composition may contribute to the reorganisation of coastal ecosystem observed at CO2 seeps globally. In its entirety, this thesis significantly contributes to our understanding of the spatial dynamics of marine microbial communities by revealing the highly deterministic nature of bacterioplankton community assembly in the coastal waters and central gyre of the South Pacific Ocean. Furthermore, the findings of this thesis highlight the dominance of stochastic processes in structuring marine protist communities across short spatial scales, which may contribute to challenges in correlating abiotic environmental variables with marine protist community composition through space. The resistance of bacterioplankton communities to ocean acidification at the fringe of the South Pacific Gyre, and subtle responses to ocean acidification at the ultra-oligotrophic centre of the South Pacific Gyre broadly support the notion that bacterioplankton communities are resilient to near-future ocean acidification. In contrast, the composition of both prokaryotic and eukaryotic biofilm communities was profoundly affected by ocean acidification, leading to the proliferation of harmful algae with potentially severe consequences for coastal marine environments.