Algae−bacteria interactions that balance the planktonic microbiome

Cirri, Emilio; Pohnert, Georg

doi:10.1111/nph.15765

Cited by 230 publications

(145 citation statements)

References 47 publications

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“…For instance, seaweeds can chemically garden beneficial microbes, facilitating normal morphogenesis and increasing disease resistance (Kessler et al 2018;Saha and Weinberger 2019), and seaweeds and corals structure their surface-associated microbiome by producing chemo-attractants and anti-bacterial compounds (Harder et al 2012;Ochsenkühn et al 2018). There are fewer examples of chemical gardening in unicellular hosts, but it seems highly likely that similar processes are in place (Gribben et al 2017;Cirri and Pohnert 2019).…”

Section: Challenges and Opportunities In Marine Holobiont Researchmentioning

confidence: 99%

A community perspective on the concept of marine holobionts: current status, challenges, and future directions

Dittami

Arboleda

Auguet

et al. 2019

Preprint

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Host-microbe interactions play crucial roles in marine ecosystems, but we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota, living together in a stable relationship, form the holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences with comparisons to terrestrial sciences where appropriate. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g. the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. The most significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This will be crucial to decipher the roles of marine holobionts in biogeochemical cycles, but also developing concrete applications of the holobiont concept e.g. to increase yield or disease resistance in aquacultures or to protect and restore marine ecosystems through management projects.

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Section: Challenges and Opportunities In Marine Holobiont Researchmentioning

confidence: 99%

A community perspective on the concept of marine holobionts: current status, challenges, and future directions

Dittami

Arboleda

Auguet

et al. 2019

Preprint

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“…Several biotic and abiotic factors have been shown to drive microbiome assembly and modulation in special compartments and organelles of multicellular eukaryotes such as squid light organs (2), coral skeletons (3), mammalian guts (4), and roots and leaves of terrestrial plants (5). In contrast, unicellular eukaryotes such as diatoms lack developmental features that can harbor microbes, yet rely heavily on essential bacterial growth factors (6)(7)(8) to proliferate and thrive in their environment. Diatoms are ubiquitous primary producers in aquatic environments that account for ∼40% of marine carbon export (9).…”

mentioning

confidence: 99%

Diatom modulation of select bacteria through use of two unique secondary metabolites

Shibl

Isaac

Ochsenkühn

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

148

112

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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.

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“…Combined with the results from the binomial regression model, these networks provide a baseline for assessing HAB microbial communities at various stages of bloom intensity. The network results also identify specific microbes (those with the strongest connections to K. brevis) for study as HAB-associated taxa that may play important roles in the intensity and duration of K. brevis blooms, potentially via chemical interdependencies similar to those common in other phytoplankton-bacteria interactions (Seyedsayamdost et al, 2011;Amin et al, 2015;Seymour et al, 2017;Cirri & Pohnert, 2019).…”

Section: Discussionmentioning

confidence: 95%

“…The latter play major roles in marine carbon and nitrogen cycles and act as agents of ecological disturbance, including through harmful algal blooms (HABs) (Field et al, 1998;Mills & Arrigo, 2010). Phytoplankton-bacterial associations include a range of mutualistic, antagonistic, and commensal interactions (Seymour et al, 2017;Cirri & Pohnert, 2019) and bacterioplankton communities change in taxonomic of algal blooms. Both molecular and metabolomic data are highly complex and traditional ecological statistics are often unsuited to analyzing diversity patterns (Thorsen et al, 2016;Tsilimigras & Fodor, 2016;Gloor et al, 2017;Weiss et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Microbial and chemical dynamics of a toxic dinoflagellate bloom

Patin

Brown

Chebli

et al. 2020

PeerJ

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Harmful Algal Blooms (HABs) exert considerable ecological and economic damage and are becoming increasingly frequent worldwide. However, the biological factors underlying HABs remain uncertain. Relationships between algae and bacteria may contribute to bloom formation, strength, and duration. We investigated the microbial communities and metabolomes associated with a HAB of the toxic dinoflagellate Karenia brevis off the west coast of Florida in June 2018. Microbial communities and intracellular metabolite pools differed based on both bacterial lifestyle and bloom level, suggesting a complex role for blooms in reshaping microbial processes. Network analysis identified K. brevis as an ecological hub in the planktonic ecosystem, with significant connections to diverse microbial taxa. These included four flavobacteria and one sequence variant unidentified past the domain level, suggesting uncharacterized diversity in phytoplankton-associated microbial communities. Additionally, intracellular metabolomic analyses associated high K. brevis levels with higher levels of aromatic compounds and lipids. These findings reveal water column microbial and chemical characteristics with potentially important implications for understanding HAB onset and duration.

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Algae−bacteria interactions that balance the planktonic microbiome

Cited by 230 publications

References 47 publications

A community perspective on the concept of marine holobionts: current status, challenges, and future directions

A community perspective on the concept of marine holobionts: current status, challenges, and future directions

Diatom modulation of select bacteria through use of two unique secondary metabolites

Microbial and chemical dynamics of a toxic dinoflagellate bloom

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