Incubation with macroalgae induces large shifts in water column microbiota, but minor changes to the epibiota of co‐occurring macroalgae

Abstract

Macroalgae variably promote and deter microbial growth through release of organic carbon and antimicrobial compounds into the water column. Consequently, macroalgae influence the microbial composition of the surrounding water column and biofilms on nearby surfaces. Here, we use manipulative experiments to test the hypotheses that (i) Nereocystis luetkeana and Mastocarpus sp. macroalgae alter the water column microbiota in species-specific manner, that (ii) neighbouring macroalgae alter the bacterial communities on the surface (epibiota) of actively growing Nereocystis luetkeana meristem fragments (NMFs), and that (iii) neighbours alter NMF growth rate. We also assess the impact of laboratory incubation on macroalgal epibiota by comparing each species to wild counterparts. We find strong differences between the Nereocystis and Mastocarpus epibiota that are maintained in the laboratory. Nereocystis and Mastocarpus alter water column bacterial community composition and richness in a species specific manner, but cause only small compositional shifts on NMF surfaces that do not differ by species, and do not change richness. Co-incubation with macroalgae results in significant change in abundance of fivefold more genera in the water column compared to NMF surfaces, although the direction (i.e., enrichment or reduction) of shift is generally consistent between the water and NMF surfaces. Finally, NMFs grew during the experiment, but growth did not depend on the presence or identity of neighbouring macroalgae. Thus, macroalgae exhibit a strong and species-specific influence on the water column microbiota, but a much weaker influence on the epibiota of neighbouring macroalgae. Overall, these results support the idea that macroalgae surfaces are highly selective and demonstrate that modulations of macroalgal microbiota operate within an overarching paradigm of host species specificity.

Kelp beds and their local effects on seawater chemistry, productivity, and microbial communities

“…Previous incubations of seawater with Nereocystis lasting 5 d in duration resulted in increased microbial diversity in the seawater (Chen and Parfrey 2018). Previous incubations of seawater with Nereocystis lasting 5 d in duration resulted in increased microbial diversity in the seawater (Chen and Parfrey 2018).…”

Editorial 2019

“…The second section featured a number of manuscripts that investigated the structure of the microbiome in an attempt to understand the drivers of microbiota community assembly and turnover. Some contributions weighed in on the role of host phylogeny vs. ecology (Erlandson, Savage, Wei, Cavender‐Bares, & Peay, ; Ivens, Gadau, Kiers, & Kronauer, 2018; Hernandez‐Gomez, Briggler, & Williams, ; Kohl, Dearing, & Bordenstein, ; Nishida & Ochman, ; Roth‐Schulze et al., ; Schuelke, Pereira, Hardy, & Bik, ), others probed how the presence of hosts themselves alters the microbiota around them (Chen & Parfrey, ; Shukla, Vogel, Heckel, Vilcinskas, & Kaltenpoth, ), one investigated patterns of co‐infection (Rock et al, ) and one documented changes in microbiota during development (Prest, Kimball, Kueneman, & McKenzie, ). A few studies in this section studied the structure of the microbiome with manipulative experiments (e.g., Chen & Parfrey, ; Erlandson et al, ; Morella, Gomez, Wang, Leung, & Koskella, ; Raymann, Bobay, & Moran, ).…”

Introduction: The host‐associated microbiome: Pattern, process and function

“…These macroalgae also shaped each others’ surface microbiota, though in a more subtle fashion. But by and large, the two focal species retained fairly distinct microbiota in the laboratory, and in the case of Nereocystis (the kelp species), across 100s of kilometres (Chen & Parfrey, ). This argues that these hosts exert strong selectivity over their microbiota (Chen & Parfrey, ) and that not all seaweeds have microbiota as taxonomically variable as those of Ulva .…”

“…But by and large, the two focal species retained fairly distinct microbiota in the laboratory, and in the case of Nereocystis (the kelp species), across 100s of kilometres (Chen & Parfrey, ). This argues that these hosts exert strong selectivity over their microbiota (Chen & Parfrey, ) and that not all seaweeds have microbiota as taxonomically variable as those of Ulva . Finally, proliferation of waterborne microbes that were exceedingly rare without hosts suggests the capacity for host‐introduced metabolites (e.g., organic carbon, antimicrobial compounds) to promote the rapid growth of weedy bacterial taxa that would otherwise persist at low levels.…”

“…They can also powerfully assess the relative roles of host vs. environment in structuring the microbiome by controlling for each and illuminate systems with highly static symbionts that are impervious to manipulation (Hu, Lukasik, Moreau, & Russell, 2014). Such studies are often particularly informative in the many cases where microbes are predominately acquired from the environment, as in seaweed surface microbiota (Chen & Parfrey, 2018), the plant rhizosphere (Deveautour, Donn, Power, Bennett, & Powell, 2018;Erlandson et al, 2018) and gut microbiota of some animals (Newell & Douglas, 2014).…”