Microbial communities in southern California kelp forests: Who is there, what they are doing, and the implications for kelp recruitment

Background/Question/Methods

Microbial communities have major effects on nutrient cycling and ecosystem health, but they are rarely included in ecosystem models. Here we focus on the kelp forests of southern California and identify ways to include microbes into kelp forest ecosystem models. We experimentally tested the effects of altered microbial abundance and composition on survival and development of gametophyte life stages of Macrocystis pyrifera. Microbial cell abundance was altered through seawater filtration, and microbial composition was altered through general and selective antibiotics. In addition, microbial communities for the experiment were sampled from two kelp forest environments with distinct anthropogenic influence, Point Loma and Santa Catalina Island, California. Because microbes are beneficial to ecosystems and their associated hosts, we hypothesized that reducing microbial abundance would detriment the settlement success and growth of M. pyrifera propagules. Furthermore, we hypothesized that microbial communities from an anthropogenically-influenced environment, Point Loma, would decrease M. pyrifera gametophyte abundance and growth due to increased microbial pathogenicity. The taxonomic composition and functional capabilities of the microbial communities sampled from Point Loma and Catalina Island were described using next-generation metagenomic sequencing. 

Results/Conclusions

Contrary to our hypothesis, reducing microbial abundance in seawater enhanced M. pyrifera propagule success. Reducing microbial abundance through filtering resulted in increased gametophyte abundance (x̅=10.222, p=0.007) and size (x̅=0.176 mm, p<0.001), compared to treatments where microbes were maintained (x̅=6.333, x̅=0.135 mm). In addition, altering the microbial community through antibiotics affected gametophyte development. Erythromycin prevented zoospore settlement and germination to gametophyte (p<0.001), while kanamycin-, ampicillin- and streptomycin-altered communities increased gametophyte abundance compared to the control group (p=0.018). Furthermore, anthropogenic influence of microbial communities differentially affected M. pyrifera propagule success. In Point Loma seawater, gametophytes were more abundant (x̅=13.667) and larger (x̅=0.413 mm) under low microbial abundance (6,200 CFUs/mL) (p<0.001), and showed a deteriorated morphology under increased microbial abundance (209,260 CFUs/ml). In contrast, in Catalina Island seawater, gametophyte abundance (x̅=13.667) and size (x̅=0.443 mm) was highest in intermediate microbial abundance (45,200 CFUs/ml) (p<0.001). Metagenomic analysis showed that quorum signal producing genes, which stimulate algal spore settlement, were present in Catalina Island microbes yet absent in Point Loma microbes, negatively influencing kelp recruitment in Point Loma treatments. Microbes determine a threshold for kelp recruitment levels and influence reproductive success of the foundation kelp species, Macrocystis pyrifera, illustrating the importance of incorporating microbial communities in kelp forest recruitment and population dynamics.