Spatial Structure of Marine Host-Associated Microbiomes: Effect of Taxonomy, Species Traits, and Study Design

Abstract

Marine host-associated microbiomes can strongly influence their host's function and are shaped by selection, dispersal, diversification, and drift. These processes can lead to spatially structured microbiomes, with potential implications for host fitness in different locations. We review the literature on marine host-associated microbiomes to identify if spatially structured microbiomes are more prevalent in certain taxonomic groups, are linked to species traits, or sampling design and methodology. The 28 papers analyzed represented 38 host species, with spatial structure detected in 75% of species, increasing to 83% when restricted to studies using high-throughput DNA sequencing. Spatial structure was detected in all coral and marine mammal microbiomes, but was less common in fish (69%) and sponges (46%). Mobile species and external tissues were more likely to show spatially structured microbiomes than sessile species and internal tissues. We found no relationship between spatial structuring and maximum distance between sampling sites, with studies on large (>1000 km) and small spatial scales (<100 km) almost as likely to show spatial structure (87% vs. 79%). Our results support using high-throughput sequencing for studying marine host-associated microbiomes due to better taxonomic resolution compared to other methods. Given the observed generality of spatially structured microbiomes, future studies should test whether microbiome variation between locations affects host fitness. Researchers should include sufficient environmental microbiome sampling and host data to distinguish host and environmental effects. This will help resolve the relative importance of selection, dispersal, diversification and drift in shaping marine host-associated microbiomes.

The microbiota of intertidal macroalgae Fucus distichus is site‐specific and resistant to change following transplant

“…These microbes play a role in modulating growth, settlement, nutrition and defence in marine hosts (Egan and Gardiner, 2016; Morris et al ., 2016; Apprill, 2017; Ugarelli et al ., 2017; Woznica and King, 2018) but microbial functions important to host biology or biogeochemical processes are often performed by diverse and functionally redundant microbial taxa (Burke et al ., 2011; Roth‐Schulze et al ., 2016; Louca et al ., 2017). Within a host species, there can be seasonal turnover in the taxonomic composition of associated microbes (the microbiota) (Bengtsson et al ., 2010; Lachnit et al ., 2011; Serebryakova et al ., 2018) and variation across geographic and/or environmental gradients (Pantos et al ., 2015; Pfister et al ., 2019; Weigel and Pfister, 2019; Schellenberg and Clarke, 2020). This taxonomic variation in time and space suggests the environment plays a strong role in the composition of host‐associated microbial communities (Adair and Douglas, 2017; Louca et al ., 2018).…”

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

“…These type of populations are typically found in eusocial animals, such as termites. Despite a long history of research on host-associated microbial communities, biogeographical patterns of host-associated microbiomes within one climatic zone are not well investigated and understood (Härer & Rennison, 2023;Schellenberg & Clarke, 2020), especially for organisms with relatively unstructured gastrointestinal microbiomes.…”