Oxygen metabolism shapes microbial settlement on photosynthetic kelp blades compared to artificial kelp substrates

Abstract

Summary We examined factors shaping community assembly of the bull kelp (Nereocystis luetkeana) microbiome by comparing microbial biofilm formation on photosynthetic kelp blade tissues and artificial kelp substrates (‘agar substrates’) deployed into a kelp forest. New kelp blade tissues were colonized by markedly distinct microbial taxa relative to agar substrates during the same time interval, even when agar substrates were infused with N. luetkeana blades, suggesting that microbial settlement onto kelp surfaces is more than just attraction to a polysaccharide‐rich surface. Further, common seawater taxa such as Colwellia sp. and Psychromonas sp. became abundant on agar substrates but avoided new kelp blade tissues, indicating that host‐specific factors may deter certain surface‐associated marine microbial taxa. Over two‐thirds of the bacterial taxa in the kelp microbiome were associated with strictly aerobic metabolisms; thus, photosynthetic production of O2 may favour aerobic microbial metabolisms. While living kelp blades primarily recruited aerobic microbes, including the obligate aerobe Granulosicoccus sp., microbes that colonized agar substrates were predominantly facultative anaerobes. We also found that infusion of kelp tissues into agar substrates altered microbial community composition and lowered taxonomic diversity relative to control agar substrates, suggesting that non‐living components of the kelp blade also impact microbial community assembly.

The diversity and functional capacity of microbes associated with coastal phototrophs

“…Blade tissue interacts with the water column and is likely more oxygenated than rhizome tissue or sediments, though a previous study suggests there can also be a 60% reduction in oxygen along the immediate surface of kelp blades (67), and along the mucus layer where some kelp-associated bacteria reside (6). Over two-thirds of the bacterial taxa on blades of N. luetkeana belonged to families associated with obligately aerobic metabolisms, demonstrating the role of oxygen in shaping phototroph-associated microbial communities (68). The sediment surrounding the rhizomes of Phyllospadix spp .…”

More than a stick in the mud: Eelgrass leaf and root bacterial communities are distinct from those on physical mimics

“…This contrasts with mimicked environments from other marine organismal phyllospheres. Recent work in kelp indicated an enrichment of common seawater taxa on artificial substrate (agar infused with and without kelp), no difference in taxonomic diversity on artificial substrates compared to kelp, and increases in aerobic taxa on the surface of kelp blades (Weigel and Pfister, 2021). We found none of these patterns on seagrass and seagrass mimics, instead finding no enrichment for common taxa on seagrass compared to mimics, higher taxonomic diversity on mimics, and no compelling evidence that compositional differences we observed were due to differences in aerobic conditions.…”

Eco‐phylogenetic analyses reveal divergent evolution of vitaminB12metabolism in the marine bacterial family ‘Psychromonadaceae’

“…by 16S rRNA full‐length sequences comparisons, along with several other Gammaproteobacterial genera, e.g. Shewanella and Vibrio that are commonly found in the epiphytic sphere of macroalgae (Saha and Weinberger, 2019; Weigel and Pfister, 2021). After purification, the strain E26 was routinely grown in nutrient broth (LB; BD) supplemented with 2% (wt./vol.)…”

“…Owing to the fluctuating marine environment, macroalgae establish intimated associations with other living organisms to sustain their environmental fitness (Li et al ., 2016; Li et al ., 2017). The macroalgal surface, being rich sources of polysaccharides, oxygen and nutrients, creates a specific ecological niche differing from the ambient water column, thereby rendering an unique microenvironment for a myriad of surface‐associated heterotrophic microbial colonizers that compose the epiphytic microbiota (Saha and Weinberger, 2019; Weigel and Pfister, 2021). In addition to the host selection, the maintenance of compositional integrity and functional stability of epiphytic microbiota can be also modulated by consistent meta–metabolic interactions as seen in animal microbiota (Danchin and Braham, 2017).…”

“…In addition to these extremophiles, other Psychromonas spp. can be also found in normal marine environment including coastal ocean (Enke et al ., 2019), column water (Groudieva et al ., 2003), and associated with marine macroalgae (Bunse et al ., 2021; Thomas et al ., 2021; Weigel and Pfister, 2021). Another genus Motilimonas (Ling et al ., 2017) from a yet‐to‐be‐assigned family ( Incertae sedis ) within the order Alteromonadales includes three validly published species, i.e.…”