Metagenomic analysis provides functional insights into seasonal change of a non-cyanobacterial prokaryotic community in temperate coastal waters.

Kaoru Matsumoto,Tan Engkong,Shuichi Asakawa,Shigeho Kakehi,Yoji Igarashi,Yukiko Taniuchi,Tomoko Sakami,Shugo Watabe,Akira Kuwata,Takanori Kobayashi,Shigeharu Kinoshita,Tsuyoshi Watanabe,Yoshizumi Ishino,Takashi Gojobori,Kazuho Ikeo,Masahira Hattori,Raffaella Casotti

doi:10.1371/journal.pone.0257862

Abstract

The taxonomic compositions of marine prokaryotic communities are known to follow seasonal cycles, but functional metagenomic insights into this seasonality is still limited. We analyzed a total of 22 metagenomes collected at 11 time points over a 14-month period from two sites in Sendai Bay, Japan to obtain seasonal snapshots of predicted functional profiles of the non-cyanobacterial prokaryotic community. Along with taxonomic composition, functional gene composition varied seasonally and was related to chlorophyll a concentration, water temperature, and salinity. Spring phytoplankton bloom stimulated increased abundances of putative genes that encode enzymes in amino acid metabolism pathways. Several groups of functional genes, including those related to signal transduction and cellular communication, increased in abundance during the mid- to post-bloom period, which seemed to be associated with a particle-attached lifestyle. Alternatively, genes in carbon metabolism pathways were generally more abundant in the low chlorophyll a period than the bloom period. These results indicate that changes in trophic condition associated with seasonal phytoplankton succession altered the community function of prokaryotes. Our findings on seasonal changes of predicted function provide fundamental information for future research on the mechanisms that shape marine microbial communities.

Highlights

Prokaryotes play essential roles in oceanic biogeochemical cycles
We show that the functional gene profile of the non-cyanobacterial prokaryotic community varied seasonally along with the taxonomic composition, and report the seasonal patterns of functional gene abundance that seemed to reflect changes in nutrient condition associated with the phytoplankton population
This study provided a functional metagenomics perspective on seasonal change in coastal non-cyanobacterial prokaryotic communities

Summary

Introduction

Prokaryotes play essential roles in oceanic biogeochemical cycles. Notably, heterotrophic prokaryotes process a large part of the organic matter produced by phytoplankton and are consumed by predators, thereby sustaining nutrient recycling [1,2,3]. 16S rRNA gene sequencing has been revealed spatial and temporal diversity of marine prokaryotic community structure in relation to the environmental conditions [4,5]. The spring phytoplankton bloom is an important event that provides organic matter to heterotrophic prokaryotes, which results in increased prokaryotic production and biomass, and pronounced changes in community composition [11,12]. Some bacterial groups, such as flavobacteria and roseobacters, typically become dominant in the prokaryotic community during the phytoplankton bloom, whereas some other groups, such as pelagibacters (SAR11 clade), usually increase in abundance under low nutrient conditions during non-bloom periods [10,13]. One major factor of seasonal dynamics of prokaryotic community is considered to be variation in the suitable concentration and composition of nutrients among taxa due to diversification and specialization of their ability to utilize organic matters

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