Morphological complexity affects the diversity of marine microbiomes

Abstract

Large eukaryotes support diverse communities of microbes on their surface—epibiota—that profoundly influence their biology. Alternate factors known to structure complex patterns of microbial diversity—host evolutionary history and ecology, environmental conditions and stochasticity—do not act independently and it is challenging to disentangle their relative effects. Here, we surveyed the epibiota from 38 sympatric seaweed species that span diverse clades and have convergent morphology, which strongly influences seaweed ecology. Host identity explains most of the variation in epibiont communities and deeper host phylogenetic relationships (e.g., genus level) explain a small but significant portion of epibiont community variation. Strikingly, epibiota community composition is significantly influenced by host morphology and epibiota richness increases with morphological complexity of the seaweed host. This effect is robust after controlling for phylogenetic non-independence and is strongest for crustose seaweeds. We experimentally validated the effect of host morphology by quantifying bacterial community assembly on latex sheets cut to resemble three seaweed morphologies. The patterns match those observed in our field survey. Thus, biodiversity increases with habitat complexity in host-associated microbial communities, mirroring patterns observed in animal communities. We suggest that host morphology and structural complexity are underexplored mechanisms structuring microbial communities.

Microbiota-Macroalgal Relationships at a Hawaiian Intertidal Bench Are Influenced by Macroalgal Phyla and Associated Thallus Complexity

“…Thallus characteristics are key to the functional role for the macroalgae, and their development may also be directly impacted by associated microbes ( 12 , 77 ). Bacterial communities can experience a functional shift through algal life history ( 78 ), specific host identity, evolutionary history, and morphological complexity ( 13 ); therefore, these differences between hosts were expected. At ‘Ewa Beach, the thallus complexity of the host strongly influenced the community composition of the associated microbiota.…”

“…Microorganisms are ubiquitous throughout the environment and form relationships with larger eukaryotic organisms that are important in mediating host health ( 1 , 2 ). Bacterial community composition can be influenced by multiple aspects of the eukaryotic host, such as biogeography ( 3 , 4 ), morphological niche ( 3 , 5 – 9 ), health ( 10 , 11 ), and morphological complexity ( 1 , 6 , 12 – 14 ). These factors can act independently or in association with one another and can vary on an individual level ( 15 ).…”

The microbiome of the habitat‐forming brown alga Fucus vesiculosus (Phaeophyceae) has similar cross‐Atlantic structure that reflects past and present drivers1

“…Macroalgae depend upon bacteria for normal morphology (Fucus spiralis, Fries 1977; Ectocarpus sp., Tapia et al 2016; Ulva spp., Fries 1975, Provasoli and Pintner 1980, Singh et al 2011, Ghaderiardakani et al 2017, Alsufyani et al 2020, even becoming unicells when axenic (Matsuo et al 2005). The composition and structure of macroalgal microbiomes vary according to host taxonomy (Longford et al 2007, Lachnit et al 2009, Roth-Schulze et al 2018, host morphology (Lemay et al 2020), environmental gradients (Weigel and Pfister 2019, Dittami et al 2020, Quigley et al 2020, and host tissues (Quigley et al 2018(Quigley et al , 2020, but differ from the water column or adjacent substratum (Lachnit et al 2009, Quigley et al 2020.…”

Genomic Rearrangements and Sequence Evolution across Brown Algal Organelles

“…An alternative hypothesis is that these introns are spread by microbes or viruses and represent multiple infections ( Ikuta et al 2008 ) that may be removed from genomes at different rates across taxa. Brown algae have a wide range of symbionts ( Kohlmeyer and Demoulin 1981 ; Balakirev et al 2012 ; Weigel and Pfister 2019 ; Lemay et al 2021 ), parasites ( Kohlmeyer and Demoulin 1981 ; Müller et al 1999 ; Bringloe et al 2021 ), and specialist viruses—including some with very large genomes ( Müller et al 1998 , Delaroque et al 1999 )—that could act as vectors of group II introns, spreading them across brown algal taxa ( Ikuta et al 2008 ). Group II introns have also been found inconsistently in the cox 1 and rnl genes of diatom mitomes ( Pogoda et al 2019 ), suggesting that Stramenopiles may be sensitive to intron invasion at these particular loci.…”