Gill microbiome structure and function in the chemosymbiotic coastal lucinidStewartia floridana

Abstract

Lucinid bivalves harbor environmentally acquired, chemosynthetic, gammaproteobacterial gill endosymbionts. Lucinid gill microbiomes, which may contain other gammaproteobacterial and/or spirochete taxa, remain under-sampled. To understand inter-host variability of the lucinid gill microbiome, specifically in the bacterial communities, we analyzed the microbiome content of Stewartia floridana collected from Florida. Sampled gills contained a monospecific gammaproteobacterial endosymbiont expressing lithoautotrophic, mixotrophic, diazotrophic, and C1 compound oxidation-related functions previously characterized in similar lucinid species. Another low-abundance Spirochaeta-like species in ∼72% of the sampled gills was most closely related to Spirochaeta-like species in another lucinid Phacoides pectinatus and formed a clade with known marine Spirochaeta symbionts. The spirochete expressed genes were involved in heterotrophy and the transport of sugars, amino acids, peptides, and other substrates. Few muscular and neurofilament genes from the host and none from the gammaproteobacterial and spirochete symbionts were differentially expressed among quadrats predominantly covered with seagrass species or 80% bare sand. Our results suggest that spirochetes are facultatively associated with S. floridana, with potential scavenging and nutrient cycling roles. Expressed stress- and defense-related functions in the host and symbionts also suggest species-species communications, which highlight the need for further study of the interactions among lucinid hosts, their microbiomes, and their environment.

Metabolically-versatile Ca. Thiodiazotropha symbionts of the deep-sea lucinid clam Lucinoma kazani have the genetic potential to fix nitrogen

“…Following previous studies [ 12 , 13 , 18 , 19 ], our data suggests that the use of methanol, formate, and hydrogen may support the energy metabolism in Ca. T. gloverae ex.…”

“…Thiodiazotropha fuels carbon fixation via the Calvin–Benson–Bassham (CBB) cycle primarily using the oxidation of sulfide, as well as other inorganic sulfur compounds. Yet, their energy sources extend beyond sulfur and may include the oxidation of hydrogen, methanol and formate using electron acceptors such as oxygen and nitrate [ 12 , 13 , 18 , 19 ]. Several Ca.…”

Sulfur oxidation and reduction are coupled to nitrogen fixation in the roots of the salt marsh foundation plant Spartina alterniflora

“…Similar to what has been reported in their symbiosis with lucinid clams, the S. alterniflora symbionts highly expressed genes for sulfur oxidation, carbon fixation, and nitrogen fixation 22 , 26 . However, the presence and expression of genes for glycolysis and the TCA cycle point to a mixotrophic lifestyle, akin to what is observed in their symbiosis with lucinid clams 22 , 43 . High expression of high-affinity oxygen reductases, such as the cytochrome c oxidase cbb3-type and cytochrome bd ubiquinol oxidase, may serve as adaptations for oxygen respiration under sulfidic conditions as well as an oxygen scavenging strategy for nitrogen fixation 44 , 45 .…”

Metabolically-versatileCa.Thiodiazotropha symbionts of the deep-sea lucinid clamLucinoma kazanihave the genetic potential to fix nitrogen

“…The symbionts encoded and expressed components of the type VI secretion system (T6SS), which facilitates virulence, host immunomodulation and bactericidal activity in many bacterial lineages [85][86][87], and were previously found to be expressed by lucinid symbionts [18,19]. These contactdependent interbacterial "weapons" [88] are most likely to be involved in interactions with competing symbiont genotypes or cheaters during colonization of the host [18,84,89].…”

“…Thiodiazotropha fuels carbon fixation via the Calvin-Benson-Bassham (CBB) cycle primarily using the oxidation of sulfide, as well as other inorganic sulfur compounds. Yet, their energy sources expand beyond sulfur and may include the oxidation of hydrogen, methanol and formate using electron acceptors such as oxygen and nitrate [12, 13, 18, 19]. Several Ca.…”