Chemically Mediated Microbial “Gardening” Capacity of a Seaweed Holobiont Is Dynamic

Abstract

Terrestrial plants are known to “garden” the microbiota of their rhizosphere via released metabolites (that can attract beneficial microbes and deter pathogenic microbes). Such a “gardening” capacity is also known to be dynamic in plants. Although microbial “gardening” has been recently demonstrated for seaweeds, we do not know whether this capacity is a dynamic property in any aquatic flora like in terrestrial plants. Here, we tested the dynamic microbial “gardening” capacity of seaweeds using the model invasive red seaweed Agarophyton vermiculophyllum. Following an initial extraction of surface-associated metabolites (immediately after field collection), we conducted a long-term mesocosm experiment for 5 months to test the effect of two different salinities (low = 8.5 and medium = 16.5) on the microbial “gardening” capacity of the alga over time. We tested “gardening” capacity of A. vermiculophyllum originating from two different salinity levels (after 5 months treatments) in settlement assays against three disease causing pathogenic bacteria and seven protective bacteria. We also compared the capacity of the alga with field-collected samples. Abiotic factors like low salinity significantly increased the capacity of the alga to deter colonization by pathogenic bacteria while medium salinity significantly decreased the capacity of the alga over time when compared to field-collected samples. However, capacity to attract beneficial bacteria significantly decreased at both tested salinity levels when compared to field-collected samples. Dynamic microbial “gardening” capacity of a seaweed to attract beneficial bacteria and deter pathogenic bacteria is demonstrated for the first time. Such a dynamic capacity as found in the current study could also be applicable to other aquatic host–microbe interactions. Our results may provide an attractive direction of research towards manipulation of salinity and other abiotic factors leading to better defended A. vermiculophyllum towards pathogenic bacteria thereby enhancing sustained production of healthy A. vermiculophyllum in farms.

Host genetics, phenotype and geography structure the microbiome of a foundational seaweed

“…Many host or environmental factors were not measured in this study but may also significantly influence microbial communities, such as secretion of specific carbohydrates and proteins (Lachnit et al, 2011; Steinberg and De Nys, 2002), antimicrobial secondary metabolites or differences in photosynthetic yield (which indeed varied across populations). Future studies comparing genetic measures identified here with more localized chemical and isotopic signatures of the hosts may reveal other drivers of host‐associated microbiota (e.g., Bengtsson et al, 2011; Saha et al, 2020; Weigel and Pfister, 2021). Finally, surface‐associated microbial communities can vary between thallus regions (Ihua et al, 2020) and also can change dramatically over the course of development in many organisms (McFall‐Ngai et al, 2013; Yatsunenko et al, 2012).…”

“…Phenotypic variation was high at this site, particularly for morphological characteristics and levels of grazing (see Figure host or environmental factors were not measured in this study but may also significantly influence microbial communities, such as secretion of specific carbohydrates and proteins (Lachnit et al, 2011;Steinberg and De Nys, 2002), antimicrobial secondary metabolites or differences in photosynthetic yield (which indeed varied across populations). Future studies comparing genetic measures identified here with more localized chemical and isotopic signatures of the hosts may reveal other drivers of host-associated microbiota (e.g., Bengtsson et al, 2011;Saha et al, 2020;Weigel and Pfister, 2021).…”

“…Recent evidence suggests that different seaweed microbial communities can also be strongly associated with differences in host condition (Campbell et al, 2011(Campbell et al, , 2015Marzinelli et al, 2015;Qiu et al, 2019). While it is often reported that seaweedassociated microbial communities are structured by functional traits rather than taxonomy (Burke et al, 2011), recent work on brown and red seaweeds has shown that some seaweed hosts do indeed exert strong selectivity over their microbiota (Chen & Parfrey, 2018;Saha et al, 2020;Weigel & Pfister, 2019). The mechanisms behind this selectivity, however, remain unknown.…”

The seaweed holobiont: from microecology to biotechnological applications

“…Macroalgae and their epiphytic bacteria interact as a functional entity, and their interactions can improve seaweed health, growth, disease suppression and adaptation to environmental stressors (Egan et al ., 2013 ; Schmidt and Saha, 2021 ). Chemical ‘gardening’ of protective microbes by seaweed has even been demonstrated, which in turn enhances the sustainable production of seaweeds (Saha and Weinberger, 2019 ; Saha et al ., 2020 ). Consequently, the associated increased seaweed biomass in the environment can be used for feeds, biofuels and fertilizers.…”

Image-Based Analysis and Quantification of Biofouling in Cultures of the Red Alga Asparagopsis taxiformis

“…Both micro and macroalgae are prone to pathogenic microbial and viral contamination (Zhu et al 2020;Behera et al 2022). It should be noted, however, that in some cases, "contaminating" microorganisms have been shown to function as symbionts that can improve algal growth and performance (Amaral et al 2013;Wichard 2022), and have even been shown to be "farmed" by seaweed to some extent (Saha et al 2020).…”