Host genotype structures the microbiome of a globally dispersed marine phytoplankton

Abstract

Phytoplankton support complex bacterial microbiomes that rely on phytoplankton-derived extracellular compounds and perform functions necessary for algal growth. Recent work has revealed sophisticated interactions and exchanges of molecules between specific phytoplankton–bacteria pairs, but the role of host genotype in regulating those interactions is unknown. Here, we show how phytoplankton microbiomes are shaped by intraspecific genetic variation in the host using global environmental isolates of the model phytoplankton host Thalassiosira rotula and a laboratory common garden experiment. A set of 81 environmental T. rotula genotypes from three ocean basins and eight genetically distinct populations did not reveal a core microbiome. While no single bacterial phylotype was shared across all genotypes, we found strong genotypic influence of T. rotula, with microbiomes associating more strongly with host genetic population than with environmental factors. The microbiome association with host genetic population persisted across different ocean basins, suggesting that microbiomes may be associated with host populations for decades. To isolate the impact of host genotype on microbiomes, a common garden experiment using eight genotypes from three distinct host populations again found that host genotype influenced microbial community composition, suggesting that a process we describe as genotypic filtering, analogous to environmental filtering, shapes phytoplankton microbiomes. In both the environmental and laboratory studies, microbiome variation between genotypes suggests that other factors influenced microbiome composition but did not swamp the dominant signal of host genetic background. The long-term association of microbiomes with specific host genotypes reveals a possible mechanism explaining the evolution and maintenance of complex phytoplankton–bacteria chemical exchanges.

The microbiome of the dinoflagellate Prorocentrum cordatum in laboratory culture and its changes at higher temperatures

“…In diatoms, the assembly of the phycosphere microbiome has been the subject of many studies, with the seeding community, genotype of host species or strain, and bacterial competition being the most important parameters affecting the resulting microbiome composition ( Whittaker and Rynearson, 2017 ; Ajani et al, 2018 ; Behringer et al, 2018 ; Stock et al, 2022 ). Our finding is strikingly similar to a study of the diatom Thalassiosira rotula ( Ahern et al, 2021 ) showing that the diatom host genotype was the strongest determinant of microbial community composition, which they termed genotype filtering ( Ahern et al, 2021 ), while geographic location played a minor role. In our experiment, we are observing the outcome of co-adaptation between host and microbiome after many years of co-culturing under stable conditions, but such genotype filtering has nevertheless been observed after many years ( Barreto Filho et al, 2021 ).…”

Bacterial exudates as growth‐promoting agents for the cultivation of commercially relevant marine microalgal strains

“…and on the phytoplankton genetics (Ahern et al, 2021;Seyedsayamdost et al, 2011). To our knowledge, this study presents the first examination of Phaeobacter spp.…”

“…For Phaeobacter spp. the production of these functional molecules in co‐culture (i.e., microalgae) is known to be dependent on the phase of phytoplankton growth (i.e., Jekyll and Hyde effect) and on the phytoplankton genetics (Ahern et al, 2021; Seyedsayamdost et al, 2011). To our knowledge, this study presents the first examination of Phaeobacter spp.…”

Emergent community architecture despite distinct diversity in the global whale shark (Rhincodon typus) epidermal microbiome

“…Drivers of the microbiome at the population level may be due to inherent host-metabolic difference, or factors that co-vary with whale shark populations, such as global regions utilized by the sharks, as discussed above. Studies in other oceanic species, such as sponges, show both population structure 34 and haplotypes within phytoplankton populations 44 to be a source of in uence on the microbiome, perhaps even to a greater extent than environmental factors. Whale sharks have diverse haplotype structures 45 which may be an important predictor of microbiome structure observed across aggregations.…”