Comparative mitochondrial and chloroplast genomics of a genetically distinct form of Sargassum contributing to recent "Golden Tides" in the Western Atlantic

Abstract

Over the past 5 years, massive accumulations of holopelagic species of the brown macroalga Sargassum in coastal areas of the Caribbean have created "golden tides" that threaten local biodiversity and trigger economic losses associated with beach deterioration and impact on fisheries and tourism. In 2015, the first report identifying the cause of these extreme events implicated a rare form of the holopelagic species Sargassum natans (form VIII). However, since the first mention of S. natans VIII in the 1930s, based solely on morphological characters, no molecular data have confirmed this identification. We generated full-length mitogenomes and partial chloroplast genomes of all representative holopelagic Sargassum species, S. fluitans III and S. natans I alongside the putatively rare S. natans VIII, to demonstrate small but consistent differences between S. natans I and VIII (7 bp differences out of the 34,727). Our comparative analyses also revealed that both S. natans I and S. natans VIII share a very close phylogenetic relationship with S. fluitans III (94- and 96-bp differences of 34,727). We designed novel primers that amplified regions of the cox2 and cox3 marker genes with consistent polymorphic sites that enabled differentiation between the two S. natans forms (I and VIII) from each other and both from S. fluitans III in over 150 Sargassum samples including those from the 2014 golden tide event. Despite remarkable gene synteny and sequence conservation, the three Sargassum forms differ in morphology, ecology, and distribution patterns, warranting more extensive interrogation of holopelagic Sargassum genomes as a whole.

Keywords: Sargasso Sea; accumulations; chloroplast genome; macroalgae; mitogenome; strandings.

Figure 1

Map of sampling locations where we collected Sargassum (yellow dots with black centers), including open‐ocean Atlantic and Caribbean, as well as specimens collected from the shore (Caribbean and Cape Cod, USA). Stations where Sargassum was absent from net tows are shown as blue dots, and locations of mitogenome samples as red asterisks. The heatmap that overlies from approximately 38–63°W and 0–22°N depicts estimates of Sargassum accumulations from satellite data integrated over the 12‐day period coincident with the timing of the sample collection in that region. The scale of the heatmap at the lower right shows percent of the ocean surface covered by Sargassum from 0% to >0.1% (satellite data courtesy of University of South Florida Oceanography Lab, http://optics.marine.usf.edu). The yellow line graph at the bottom of the figure shows Sargassum quantity from the cruise net tows, showing the peak around 50°W and good correspondence with estimated densities from the satellite data

Figure 2

The most common forms of holopelagic Sargassum found in Atlantic: (a) herbarium specimen of Sargassum natans I from Parr's collection showing characteristic spine‐like appendages on vesicles; (b) herbarium specimen of Sargassum fluitans III from Parr's collection showing characteristic axis thorns; (c) herbarium specimen of S. natans VIII from Parr's collection showing neither spine‐like appendages nor thorns; (d) live fragment of S. natans VIII from sample used for one of the sequenced mitogenomes that matches Parr's morphological description of S. natans VIII. Scale bars are 1 cm. Herbarium images a, b, c from the Peabody Museum of Natural History, Yale University (YU); peabody.yale.edu

Figure 3

A maximum‐likelihood‐inferred phylogeny of mitogenomes from all available Sargassum species alongside the holopelagic species sequenced in this study (in bold). Scale bar represents evolutionary distance, and numbers at the nodes represent bootstrap confidence values. GenBank numbers follow the names of published mitogenomes