Spatial patterns in host-associated and free-living bacterial communities across six temperate estuaries

Abstract

A major goal of microbial ecology is to establish the importance of spatial and environmental factors in driving community variation. Their relative importance likely varies across spatial scales, but focus has primarily been on free-living communities within well-connected aquatic environments rather than less connected island-like habitats such as estuaries, and key host-associated communities within these systems. Here we sampled both free-living (seawater and sediment) and host-associated (estuarine fish hindgut microbiome, Pelates sexlineatus) communities across six temperate Australian estuaries spanning ∼500 km. We find that spatial and environmental factors have different influences on these communities, with seawater demonstrating strong distance-decay relationships (R = -0.69) and significant associations with a range of environmental variables. Distance-decay relationships were weak for sediment communities but became stronger over smaller spatial scales (within estuaries, R = -0.5) potentially reflecting environmental filtering across biogeochemical gradients or stochastic processes within estuary sediments. Finally, P. sexlineatus hindgut microbiome communities displayed weak distance-decay relationships (R = -0.36) and limited variation explained by environmental variables, indicating the significance of host-related factors in driving community variation. Our findings provide important ecological insights into the spatial distributions and driving forces of both free-living and host-associated bacterial patterns across temperate estuarine systems.

Distinct biogeographical patterns in snail gastrointestinal tract bacterial communities compared with sediment and water

“…As expected, based on the results reported in previous invertebrate gut microbiome analysis (Sullam et al, 2015 ; Suzzi et al, 2023 ) the number of ASV in the gastrointestinal tract did not differ significantly between samples from different biogeographic regions (Figure 5 ), but were lower compared with water or sediment. In all gastrointestinal samples, Gammaproteobacteria (23.3%–46.3%), Alphaproteobacteria (13.0%–22.8%), and Planctomycetes (3.0%–16.6%) were dominant.…”

“…However, these ASVs were only lowly abundant in the samples from Denmark ( Mycoplasma [0.1%], Luteolibacter [1.9%], and Aeromonas [0.1%]) and Germany ( Mycoplasma [0.1%], Luteolibacter [1.3%], and Aeromonas [0.0%]) suggesting that they were not available during initial colonization. A strong influence of environmental factors and low turnover rates were also observed in previous studies of gastrointestinal bacterial communities in estuarine fishes (Suzzi et al, 2023 ).…”

“…The low turnover rates of the gastrointestinal tract indicated that the similarity of the gastrointestinal tract microbiome is more constant at larger distances compared with water or sediment bacterial communities. Hence, the gastrointestinal tract provides unique conditions for selecting specific bacterial communities rather than environmental factors (Suzzi et al, 2023 ; Taylor et al, 2005 ). However, we sampled only comparable environments (lakes, rivers) on a relatively small geographic scale (max 1245 km).…”

“…Highly diverse and specific host‐associated microbial communities are important reservoirs for biodiversity (Taylor et al, 2005 ). Aquatic host organisms offer distinct environmental conditions for microbial colonization compared to the surrounding environment (Suzzi et al, 2023 ). They function as habitat islands (MacArthur & Wilson, 2001 ) and provide unique ecological niches.…”