Gut Microbiota Associated With Different Sea Lamprey (Petromyzon marinus) Life Stages

Sea lamprey (SL; Petromyzon marinus), one of the oldest living vertebrates, have a complex metamorphic life cycle. Following hatching, SL transition into a microphagous, sediment burrowing larval stage, and after 2–10+ years, the larvae undergo a dramatic metamorphosis, transforming into parasitic juveniles that feed on blood and bodily fluids of fishes; adult lamprey cease feeding, spawn, and die. Since gut microbiota are critical for the overall health of all animals, we examined the microbiota associated with SLs in each life history stage. We show that there were significant differences in the gut bacterial communities associated with the larval, parasitic juvenile, and adult life stages. The transition from larval to the parasitic juvenile stage was marked with a significant shift in bacterial community structure and reduction in alpha diversity. The most abundant SL-associated phyla were Proteobacteria, Fusobacteria, Bacteroidetes, Verrucomicrobia, Actinobacteria, and Firmicutes, with their relative abundances varying among the stages. Moreover, while larval SL were enriched with unclassified Fusobacteriaceae, unclassified Verrucomicrobiales and Cetobacterium, members of the genera with fastidious nutritional requirements, such as Streptococcus, Haemophilus, Cutibacterium, Veillonella, and Massilia, were three to four orders of magnitude greater in juveniles than in larvae. In contrast, adult SLs were enriched with Aeromonas, Iodobacter, Shewanella, and Flavobacterium. Collectively, our findings show that bacterial communities in the SL gut are dramatically different among its life stages. Understanding how these communities change over time within and among SL life stages may shed more light on the role that these gut microbes play in host growth and fitness.

Novel “omega muscle units” in superficial body-wall myotomes during metamorphosis in the northern brook lamprey (Ichthyomyzon fossor)

Lampreys transform from sedentary filter feeders to more mobile adults through a dramatic metamorphosis that includes remodeling of head muscle and skeletal systems. Metamorphic modifications of body-wall myotomes that could support changes in swimming behavior from larvae to adults have not been previously reported. Thus, transverse sections of northern brook lamprey (Ichthyomyzon fossor Reighard and Cummins, 1916) in larval (n = 4), metamorphosing (n = 3), and adult (n = 2) stages were used to investigate the architecture of body-wall muscle and to detect whether Pax7 and MyoD, proteins important in myogenesis, were co-localized in any muscle nuclei. In addition to myotomal complexity of muscle units composed of parietal and central fibers, there was a novel pattern of omega-shaped muscle units with curves of muscle fibers in the superficial mid-body myotome in metamorphosing lamprey. Small satellite-like cells were identified on central fibers in metamorphosing and adult lamprey muscle using routine histology and immunolocalization of Pax7 and MyoD with antibodies that specifically detect mammalian and teleost proteins. Transient “omega muscle units” may be a marker for impending myotomal growth and increasing swimming efficiency during maturation, possibly restricted to metamorphosis. Finding satellite-like cells suggests that Pax7 and MyoD may have distinctive roles in lamprey myogenesis.

The future of barriers and trapping methods in the sea lamprey (Petromyzon marinus) control program in the Laurentian Great Lakes

A major duty of the Great Lakes Fishery Commission (GLFC), created in 1955, was the development a program of eradication or management of sea lamprey populations in the Great Lakes for the protection of the Great Lakes fishery. Beginning in the 1980s the GLFC shifted sea lamprey control to an integrated pest management model seeking to deploy control measures which target multiple life stages. Currently control efforts focus on limiting the area of infestation using barriers to migratory adults and eradication of larvae from streams using selective pesticides. Feedback on program effectiveness is obtained by trapping migratory adult lamprey at a series of index sites around the basin. The GLFC continues to support multiple research initiatives to develop additional control, improve current control measures, and further advance the sea lamprey control program. During the past six decades sea lamprey control in the Great Lakes has evolved as the research program has identified technological advances. Here we summarize the current state and recent advancements for two of the sea lamprey control program’s core elements, barriers and traps, highlight challenges to be addressed to continue the advancement of these program elements, and provide a series of research questions to spur interest within the research community. Further, because considerable information about these program elements is scattered among grey literature and technical reports, we summarize the history of barriers and traps in sea lamprey control in the included appendices to provide relevant program background to anyone interested in pursuing these research topics.

Swimming rhythm generation in the caudal hindbrain of the lamprey

The spinal cord has been well established as the site of generation of the locomotor rhythm in vertebrates, but studies have suggested that the caudal hindbrain in larval fish and amphibians can also generate locomotor rhythms. Here, we investigated whether the caudal hindbrain of the adult lamprey ( Petromyzon marinus and Ichthyomyzon unicuspis) has the ability to generate the swimming rhythm. The hindbrain-spinal cord transition zone of the lamprey contains a bilateral column of somatic motoneurons that project via the spino-occipital (S-O) nerves to several muscles of the head. In the brainstem-spinal cord-muscle preparation, these muscles were found to burst and contract rhythmically with a left-right alternation when swimming activity was evoked with a brief electrical stimulation of the spinal cord. In the absence of muscles, the isolated brainstem-spinal cord preparation also produced alternating left-right bursts in S-O nerves (i.e., fictive swimming), and the S-O nerve bursts preceded the bursts occurring in the first ipsilateral spinal ventral root. After physical isolation of the S-O region using transverse cuts of the nervous system, the S-O nerves still exhibited rhythmic bursting with left-right alternation when glutamate was added to the bathing solution. We conclude that the S-O region of the lamprey contains a swimming rhythm generator that produces the leading motor nerve bursts of each swimming cycle, which then propagate down the spinal cord to produce forward swimming. The S-O region of the hindbrain-spinal cord transition zone may play a role in regulating speed, turning, and head orientation during swimming in lamprey. NEW & NOTEWORTHY Although it has been well established that locomotor rhythm generation occurs in the spinal cord of vertebrates, it was unknown whether the hindbrain of the adult vertebrate nervous system can also generate the locomotor rhythm. Here, we show that the isolated hindbrain-spinal cord transition zone of adult lamprey can generate the swimming rhythm. In addition, the swimming bursts of the hindbrain lead the bursts occurring in the first segment of the spinal cord.

Behavioral Responses of Pacific Lamprey to Alarm Cues

Pacific lamprey (Entosphenus tridentatus), an anadromous ectoparasite, faces several challenges during adult migration to spawning grounds. Developing methods to address these challenges is critical to the success of ongoing conservation efforts. The challenges are diverse, and include anthropogenic alterations to the ecosystem resulting in loss of habitat, impassable barriers such as dams, climate change impacts, and altered predator fields. We conducted a behavioral study to understand how adult migrating Pacific lamprey respond to potential alarm cues: White Sturgeon (Acipenser transmontanus), human saliva, decayed Pacific lamprey, and river otter (Lontra canadensis). Research has shown that some species of lamprey can be guided to a location using odors and similar cues may be useful as a management tool for Pacific lamprey. Experiments were conducted over 2 nights and measured the number of entries (count) and duration of time spent (occupancy) by adult lamprey in each arm of a two-choice maze. During the first night, no odor was added to test for selection bias between arms. During the second night odor was added to one arm of the maze. Contrary to expectations, lamprey were significantly attracted to the river otter odor in both count and occupancy. No significant differences were found in the response of lamprey to the other three odors. Results from this study indicate that Pacific lamprey do respond to some odors; however, additional tests are necessary to better identify the types of odors and concentrations that elicit a repeatable response.

The Sea Lamprey as an Etiological Model for Biliary Atresia

Biliary atresia (BA) is a progressive, inflammatory, and fibrosclerosing cholangiopathy in infants that results in obstruction of both extrahepatic and intrahepatic bile ducts. It is the most common cause for pediatric liver transplantation. In contrast, the sea lamprey undergoes developmental BA with transient cholestasis and fibrosis during metamorphosis, but emerges as a fecund adult with steatohepatitis and fibrosis in the liver. In this paper, we present new histological evidence and compare the sea lamprey to existing animal models to highlight the advantages and possible limitations of using the sea lamprey to study the etiology and compensatory mechanisms of BA and other liver diseases. Understanding the signaling factors and genetic networks underlying lamprey BA can provide insights into BA etiology and possible targets to prevent biliary degeneration and to clear fibrosis. In addition, information from lamprey BA can be used to develop adjunct treatments for patients awaiting or receiving surgical treatments. Furthermore, the cholestatic adult lamprey has unique adaptive mechanisms that can be used to explore potential treatments for cholestasis and nonalcoholic steatohepatitis (NASH).