Unicellular eukaryotic phytoplankton, such as diatoms, rely on microbial communities for survival despite lacking specialized compartments to house microbiomes (e.g., animal gut). Microbial communities have been widely shown to benefit from diatom excretions that accumulate within the microenvironment surrounding phytoplankton cells, known as the phycosphere. However, mechanisms that enable diatoms and other unicellular eukaryotes to nurture specific microbiomes by fostering beneficial bacteria and repelling harmful ones are mostly unknown. We hypothesized that diatom exudates may tune microbial communities and employed an integrated multiomics approach using the ubiquitous diatom Asterionellopsis glacialis to reveal how it modulates its naturally associated bacteria. We show that A. glacialis reprograms its transcriptional and metabolic profiles in response to bacteria to secrete a suite of central metabolites and two unusual secondary metabolites, rosmarinic acid and azelaic acid. While central metabolites are utilized by potential bacterial symbionts and opportunists alike, rosmarinic acid promotes attachment of beneficial bacteria to the diatom and simultaneously suppresses the attachment of opportunists. Similarly, azelaic acid enhances growth of beneficial bacteria while simultaneously inhibiting growth of opportunistic ones. We further show that the bacterial response to azelaic acid is numerically rare but globally distributed in the world’s oceans and taxonomically restricted to a handful of bacterial genera. Our results demonstrate the innate ability of an important unicellular eukaryotic group to modulate select bacteria in their microbial consortia, similar to higher eukaryotes, using unique secondary metabolites that regulate bacterial growth and behavior inversely across different bacterial populations. Significance Phytoplankton are major primary producers in the marine environment that excrete a wide range of metabolites. These exudates support the growth of surrounding bacteria that in turn provide phytoplankton cells with resources and growth cofactors to proliferate. Unlike multicellular eukaryotes with dedicated structures housing microbiomes, mechanisms enabling unicellular eukaryotic phytoplankton hosts to modulate potential symbionts and opportunists within a natural microbial community are unknown. Exposure of a host phytoplankton cell to its natural microbial community triggers major transcriptional and metabolic reprogramming to release unique secondary metabolites that selectively enable growth and attachment of symbiotic taxa while simultaneously suppressing the colonization of nonsymbiont bacteria. These results suggest strong and highly selective microbiome-modulating strategies shared across the unicellular and multicellular eukaryotic lineages.

Corals live in a complex, multipartite symbiosis with diverse microbes across kingdoms, some of which are implicated in vital functions, such as those related to resilience against climate change. However, knowledge gaps and technical challenges limit our understanding of the nature and functional significance of complex symbiotic relationships within corals. Here, we provide an overview of the complexity of the coral microbiome focusing on taxonomic diversity and functions of well-studied and cryptic microbes. Mining the coral literature indicate that while corals collectively harbour a third of all marine bacterial phyla, known bacterial symbionts and antagonists of corals represent a minute fraction of this diversity and that these taxa cluster into select genera, suggesting selective evolutionary mechanisms enabled these bacteria to gain a niche within the holobiont. Recent advances in coral microbiome research aimed at leveraging microbiome manipulation to increase coral’s fitness to help mitigate heat stress-related mortality are discussed. Then, insights into the potential mechanisms through which microbiota can communicate with and modify host responses are examined by describing known recognition patterns, potential microbially derived coral epigenome effector proteins and coral gene regulation. Finally, the power of omics tools used to study corals are highlighted with emphasis on an integrated host–microbiota multiomics framework to understand the underlying mechanisms during symbiosis and climate change-driven dysbiosis.

Corals are threatened worldwide due to prevalence of disease and bleaching. Recent studies suggest the ability of corals to resist disease is dependent on maintaining healthy microbiomes that span coral tissues and surfaces, the holobiont. Although our understanding of the role endosymbiotic microbes play in coral health has advanced, the role surface-associated microbes and their chemical signatures play in coral health is limited. Using minimally invasive water sampling, we show that the corals Acropora and Platygyra harbor unique bacteria and metabolites at their surface, distinctly different from surrounding seawater. The surface metabolites released by the holobiont create concentration gradients at 0–5 cm away from the coral surface. These molecules are identified as chemo-attractants, antibacterials, and infochemicals, suggesting they may structure coral surface-associated microbes. Further, we detect surface-associated metabolites characteristic of healthy or white syndrome disease infected corals, a finding which may aid in describing effects of diseases.

The elemental composition of freshwater and saltwater samples around the South Pacific island of Upolu, Samoa has been investigated together with other indicators of water quality. Up to 69 elements from Li (3) to U (92) are measured in each sample, analyzed by Mattauch–Herzog-inductively coupled plasma-mass spectrometry (MH-ICP-MS). One hundred and seventy-six samples were collected from surface freshwater sources (24 rivers, two volcanic lakes, one dam) and from seawater sources from the surface to 30 m depth (45 inner reef, reef, and outer reef locations) around Upolu Island, including river mouths and estuaries. Principal component and hierarchical clustering correlation analyses were performed on quantile normalized log transformed elemental composition data to identify groups of samples with similar characteristics and to improve the visualization of the full spectrum of elements. Human activities, such as the use of herbicides and pesticides, may relate to observed elevated concentrations of some elements contained in chemicals known to have deleterious obesogenic effects on humans that may also cause coral reef decline. Furthermore, the salinity of some saltwater samples tested were very high, possibly due to climate variability, which may additionally harm the health and biodiversity of coral reefs.

Rising temperatures are devastating coral populations throughout the globe¹. The coral microbiome is believed to play a critical role in sustaining corals and enabling their adaptation to environmental changes, particularly thermal stress^2–4. A ubiquitous group of coral-associated bacteria, known as Endozoicomonas, are hypothesized to provide their host with essential metabolites⁵. However, the nature of coral-Endozoicomonas symbiosis and the role these bacteria play in adaptation to thermal stress are largely unknown. Here, we show that symbiotic Endozoicomonas adapt to the host environment by gaining the ability to degrade coral-derived steroids and Symbiodiniaceae-derived galactose while losing the ability to synthesize iron-binding siderophores, a common feature of free-living marine bacteria⁶. More importantly, under thermal stress Endozoicomonas utilizes coral-derived cholesterol partially as a carbon source while simultaneously converting it to the hormones testosterone and progesterone. Both steroids prime the innate immune system and inhibit pathogenic bacteria and fungi⁷. These findings highlight an unknown interaction between corals and their microbiome that may be critical to coral health as oceans warm up. The ability of bacteria to synthesize eukaryotic steroid hormones underscores the importance of these molecules in inter-kingdom interactions and suggests that their origin may have evolved as a result of eukaryogenesis.

Analysis of microbe diversity in freshwater resources and nearshore seawater samples of Upolu Island was performed to investigate the distribution of harmful bacteria. For this, 124 samples were collected from 23 river systems, two volcanic lakes, and 45 locations inside and outside the barrier reef of Upolu Island, Samoa. Physicochemical parameters for general water quality, detection of coliform bacteria and 16S rRNA amplicon sequencing were performed on all samples. Fecal indicator bacteria (FIB) testing indicated a wide distribution of coliform bacteria in all sampled freshwater sites with evidence of fecal coliform in most locations. Importantly, evidence of coliform bacteria was found in most seawater samples inside and along the reef, apart from those samples taken ~20 km offshore. Illumina 16S rRNA amplicon sequencing of the V4 hypervariable region confirmed the presence of various types of harmful bacterial species, namely from the Enterobacteriaceae, Enterococcae, Streptococcaceae, and Vibrionacea families. By combining the sensitivity of FIB testing and next-generation sequencing, we were able to show the extent of potential contaminations in fresh and seawater samples and simultaneously identify the potential pathogenic bacterial genera present. The wide distribution of potential harmful bacteria from river runoff or direct sewage dumping has an impact on human health, leading to many skin and intestinal diseases, and is potentially detrimental to coral reef community health.