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 j...

Full description

Bibliographic Details
Main Authors: Prince P. Mathai, Muruleedhara N. Byappanahalli, Nicholas S. Johnson, Michael J. Sadowsky
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.706683/full
id doaj-beb5e772c6e541bbb5e52b36a27d22ec
record_format Article
spelling doaj-beb5e772c6e541bbb5e52b36a27d22ec2021-09-04T10:56:19ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-09-011210.3389/fmicb.2021.706683706683Gut Microbiota Associated With Different Sea Lamprey (Petromyzon marinus) Life StagesPrince P. Mathai0Muruleedhara N. Byappanahalli1Nicholas S. Johnson2Michael J. Sadowsky3Michael J. Sadowsky4Michael J. Sadowsky5BioTechnology Institute, University of Minnesota, St. Paul, MN, United StatesU.S. Geological Survey, Great Lakes Science Center, Lake Michigan Ecological Research Station, Chesterton, IN, United StatesU.S. Geological Survey, Great Lakes Science Center, Hammond Bay Biological Station, Millersburg, MI, United StatesBioTechnology Institute, University of Minnesota, St. Paul, MN, United StatesDepartment of Soil, Water and Climate, University of Minnesota, St. Paul, MN, United StatesDepartment of Plant and Microbial Biology, University of Minnesota, St. Paul, MN, United StatesSea 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.https://www.frontiersin.org/articles/10.3389/fmicb.2021.706683/fullsea lampreyPetromyzon marinusgut microbiotalife stagesmicrobial community structure
collection DOAJ
language English
format Article
sources DOAJ
author Prince P. Mathai
Muruleedhara N. Byappanahalli
Nicholas S. Johnson
Michael J. Sadowsky
Michael J. Sadowsky
Michael J. Sadowsky
spellingShingle Prince P. Mathai
Muruleedhara N. Byappanahalli
Nicholas S. Johnson
Michael J. Sadowsky
Michael J. Sadowsky
Michael J. Sadowsky
Gut Microbiota Associated With Different Sea Lamprey (Petromyzon marinus) Life Stages
Frontiers in Microbiology
sea lamprey
Petromyzon marinus
gut microbiota
life stages
microbial community structure
author_facet Prince P. Mathai
Muruleedhara N. Byappanahalli
Nicholas S. Johnson
Michael J. Sadowsky
Michael J. Sadowsky
Michael J. Sadowsky
author_sort Prince P. Mathai
title Gut Microbiota Associated With Different Sea Lamprey (Petromyzon marinus) Life Stages
title_short Gut Microbiota Associated With Different Sea Lamprey (Petromyzon marinus) Life Stages
title_full Gut Microbiota Associated With Different Sea Lamprey (Petromyzon marinus) Life Stages
title_fullStr Gut Microbiota Associated With Different Sea Lamprey (Petromyzon marinus) Life Stages
title_full_unstemmed Gut Microbiota Associated With Different Sea Lamprey (Petromyzon marinus) Life Stages
title_sort gut microbiota associated with different sea lamprey (petromyzon marinus) life stages
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-09-01
description 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.
topic sea lamprey
Petromyzon marinus
gut microbiota
life stages
microbial community structure
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.706683/full
work_keys_str_mv AT princepmathai gutmicrobiotaassociatedwithdifferentsealampreypetromyzonmarinuslifestages
AT muruleedharanbyappanahalli gutmicrobiotaassociatedwithdifferentsealampreypetromyzonmarinuslifestages
AT nicholassjohnson gutmicrobiotaassociatedwithdifferentsealampreypetromyzonmarinuslifestages
AT michaeljsadowsky gutmicrobiotaassociatedwithdifferentsealampreypetromyzonmarinuslifestages
AT michaeljsadowsky gutmicrobiotaassociatedwithdifferentsealampreypetromyzonmarinuslifestages
AT michaeljsadowsky gutmicrobiotaassociatedwithdifferentsealampreypetromyzonmarinuslifestages
_version_ 1717815256179277824